In recent years, the impact of prenatal sound on development, notably for programming individual phenotypes for postnatal conditions, has increasingly been revealed. However, the mechanisms through which sound affects physiology and development remain mostly unexplored. Here, I gather evidence from neurobiology, developmental biology, cellular biology and bioacoustics to identify the most plausible modes of action of sound on developing embryos. First, revealing often-unsuspected plasticity, I discuss how prenatal sound may shape auditory system development and determine individuals' later capacity to receive acoustic information. I also consider the impact of hormones, including thyroid hormones, glucocorticoids and androgen, on auditory plasticity. Second, I review what is known about sound transduction to other – non-auditory – brain regions, and its potential to input on classical developmental programming pathways. Namely, the auditory pathway has direct anatomical and functional connectivity to the hippocampus, amygdala and/or hypothalamus, in mammals, birds and anurans. Sound can thus trigger both immediate and delayed responses in these limbic regions, which are specific to the acoustic stimulus and its biological relevance. Third, beyond the brain, I briefly consider the possibility for sound to directly affect cellular functioning, based on evidence in earless organisms (e.g. plants) and cell cultures. Together, the multi-disciplinary evidence gathered here shows that the brain is wired to allow multiple physiological and developmental effects of sound. Overall, there are many unexplored, but possible, pathways for sound to impact even primitive or immature organisms. Throughout, I identify the most promising research avenues for unravelling the processes of acoustic developmental programming.

Developmental plasticity, whereby the conditions encountered in early life direct the developmental processes and resulting phenotype of the individual, is a fundamental aspect of ontogeny and adaptation (Agrawal et al., 1999; Dantzer et al., 2013; Duckworth et al., 2015; Lupien, 2009; Welberg and Seckl, 2001). Extensive research in both behavioural ecology and biomedicine has shown that maternal hormones in particular can have a strong impact on offspring development (Banerjee et al., 2012; Dantzer et al., 2013; Duckworth et al., 2015; Groothuis, 2019; Groothuis and Schwabl, 2008; Lupien, 2009; Welberg and Seckl, 2001).

Glossary

Brain-derived neurotrophic factor (BDNF)

As a neurotrophic factor (which controls cell differentiation and proliferation), BDNF (and its receptor TrkB) is involved in neuronal maintenance and growth, and brain plasticity associated with learning.

Bromodeoxyuridine (BrdU)

A synthetic biomarker of neurogenesis and cell proliferation. As an analogue of thymidine, it is incorporated into DNA and allows detection of areas of DNA synthesis. BrdU can be injected into living subjects and later detected in brain sections.

Functional magnetic resonance imagery (fMRI)

A scanning technique on immobile awake subjects (e.g. humans) to identify areas of neuronal activity in the brain based on the detection of blood flow.

Hypothalamic–pituitary–adrenal (HPA) axis

The hypothalamus controls the release of adrenocorticotropic hormone (ACTH) from the anterior pituitary, which regulates the release from the adrenal glands (located above the kidneys) into the blood stream of glucocorticoid (GC) hormones (e.g. cortisol in humans, corticosterone in birds and rodents), as well as adrenaline and noradrenaline (also known as epinephrine and norepinephrine). GC can also be produced locally in the brain.

Hypothalamic–pituitary–gonadal (HPG) axis

Through the secretion of gonadotropin-releasing hormone (GnRH) by the hypothalamus, the HPG axis controls the release of luteinising hormone (LH) from the pituitary, which stimulates the release of steroid hormones (e.g. testosterone and androstenedione A4) from the gonads.

Hypothalamic–pituitary–thyroid (HPT) axis

The hypothalamus produces thyrotropin-releasing hormone (TRH) to regulate the secretion of thyroid-stimulating hormone (TSH) by the pituitary, which then controls the release of two types of thyroid hormones [triiodothyronine (T3) and tetradothyronine or thyroxine (T4)] by the thyroid gland (located in the throat).

Immediate early genes (IEGs)

Genes expressed transiently in neurons within minutes to an hour of receiving a stimulus, and which can trigger further changes, notably through their role as transcription regulating factors. There are several IEG [e.g. egr-1 (=ZENK), CFOS, ARC], often shared across species. They have been used widely to identify sound-sensitive brain regions, such as song nuclei in the avian brain.

Reactive oxygen species (ROS)

A class of molecules (e.g. hydrogen peroxide H2O2, superoxide O2) produced as a by-product of biochemical reactions, mostly by mitochondria (and chloroplasts and other organelles in plants), as well as in the cell membrane. ROS cause oxidative damage to cells when present in excess, but also have a signalling function. ROS levels are regulated by anti-oxidant enzymes (e.g. superoxide dismutase, catalase).

In recent years, prenatal sound has emerged as another source of information for embryos, which can also direct development (Fig. 1, Table 1; Mariette and Buchanan, 2016; Mariette et al., 2021; Noguera and Velando, 2019a). In particular, embryos in all major groups of oviparous taxa cue on external sounds and vibrations to flexibly adjust hatching time to risks and opportunities (Mariette et al., 2021). Vibro-acoustic cues inform on the imminence of siblings hatching such as in reptiles and birds (Vergne and Mathevon, 2008; Vince, 1964; Woolf et al., 1976), or on the risk of predation (e.g. frogs hatching to escape an egg predator: Jung et al., 2020; Warkentin, 2005) or cannibalism (e.g. by newly hatched siblings in insects: Endo et al., 2019). This plasticity in hatching time can in turn have carry-over effects on post-hatch phenotype, notably by affecting the degree of maturity at hatching (e.g. Aubret et al., 2016; Delia et al., 2019).

Fig. 1.

Developmental plasticity by prenatal sounds in vertebrates. Sound triggers a diversity of responses in embryos across taxa. In particular, in addition to permitting auditory learning and shaping auditory capacity during a sensitive prenatal period, sound allows oviparous embryos to optimise hatching time, and affects post-natal growth and begging display, as well as stress physiology. Some effects of prenatal sounds persist into adulthood, affecting individual physiology (e.g. thermoregulation) and behaviour (e.g. song learning).

Fig. 1.

Developmental plasticity by prenatal sounds in vertebrates. Sound triggers a diversity of responses in embryos across taxa. In particular, in addition to permitting auditory learning and shaping auditory capacity during a sensitive prenatal period, sound allows oviparous embryos to optimise hatching time, and affects post-natal growth and begging display, as well as stress physiology. Some effects of prenatal sounds persist into adulthood, affecting individual physiology (e.g. thermoregulation) and behaviour (e.g. song learning).

Table 1.

Some examples of the effects of sound at multiple levels of organisation, across a diversity of taxa from vertebrates to plants

Some examples of the effects of sound at multiple levels of organisation, across a diversity of taxa from vertebrates to plants
Some examples of the effects of sound at multiple levels of organisation, across a diversity of taxa from vertebrates to plants

Another independent area of research has shown that, in both birds and humans, embryos are capable of learning acoustic signals prenatally, to facilitate mother–offspring recognition at hatching/birth. In particular, in precocial birds such as quails and ducks, and in humans, newborns discriminate their mother’s vocalisations heard prenatally against those of another unfamiliar female (Bertin et al., 2009; Decasper and Fifer, 1980; Gottlieb, 2002; Herrington et al., 2015). Prenatal acoustic experience may also influence vocal production in altricial birds and humans (Colombelli-Negrel et al., 2012; Mampe et al., 2009; Mariette et al., 2021). For example, in superb fairy wrens (Malurus cyaneus), it has been suggested that nestling begging calls are partly learnt prenatally, as they resemble a syllable of the ‘incubation call’ produced by incubating females (Colombelli-Negrel et al., 2012). In zebra finches (Taeniopygia castanotis), developmental shifts triggered by parental ‘heat-calls’ during incubation (see below) lead (indirectly) to changes in male song learning and song preferences in adulthood (Katsis et al., 2023, 2018).

Most strikingly, sound may also provide anticipatory cues to embryos, forecasting postnatal conditions and allowing embryos to adjust their phenotype accordingly. This was first demonstrated in the zebra finch, where parents produce a peculiar ‘heat-call’ during incubation, only at high temperatures (Mariette and Buchanan, 2016, 2019). Exposure to such heat calls prenatally leads to a range of morphological and physiological changes in nestlings and then adults, in relation to the temperature they experience. Specifically, heat-call-exposed individuals grow less in hot nests than individuals exposed prenatally to control calls (Mariette and Buchanan, 2016), which may be triggered by a shift in mitochondrial function (Udino et al., 2021). Such adjustment of growth to temperature then leads to higher reproductive success throughout adulthood, which suggests that developmental programming by parental heat-calls is adaptive (Mariette and Buchanan, 2016). In addition, heat-call-exposed individuals have hotter thermal preferences and higher heat tolerance at adulthood, and also a different panting strategy that could potentially reduce heat accumulation (Mariette and Buchanan, 2016; Pessato et al., 2022; Udino and Mariette, 2022).

In another species, and a different ecological context, adult calls heard prenatally also shape postnatal growth trajectories: in the yellow-legged seagull (Larus michahellis), prenatal exposure to adult alarm calls (typically triggered by predator presence) alters hatching time and many hatchling traits, including growth, corticosterone levels, red blood cell DNA methylation and telomere length (Noguera and Velando, 2019a,b). Exposed individuals were also more prone to crouch in response to alarm calls postnatally (Noguera and Velando, 2019a). While these are so far the only two known cases of developmental programming by anticipatory prenatal acoustic signals, it is likely to occur widely, including in non-avian species. Notably, sound may provide anticipatory cues at other transitions between developmental stages (Mariette et al., 2021). For example, in two species of crickets, male song rate and complexity – indicative of the current level of sexual competition or opportunities – affect time to emergence (from nymph to adulthood), but also differential investment in sexual traits, in both males and females (Bailey et al., 2010; Kasumovic et al., 2011).

While some downstream mechanisms may be shared (see below; Mariette et al., 2021), sound differs from maternal biochemical cues in several important ways in the context of developmental programming and its adaptive value. From the examples above, it is apparent that sound can convey very accurate information, by signalling a particular stressor (e.g. predation, competition) rather than broadly indicating challenging environmental conditions (for example, as high maternal corticosterone levels would; e.g. Dantzer et al., 2013). In addition, the time of delivery of acoustic cues may also bring greater accuracy. Acoustic transmission occurs towards the end of embryonic development (Mariette, 2020). By contrast, in oviparous species, maternal biochemical cues can only be delivered during egg formation before laying (Groothuis and Schwabl, 2008), which may be too early to predict some postnatal conditions. Moreover, vocal communication may affect family evolutionary conflict and cooperation, as sound allows bypassing the ‘maternal bottleneck’ in information flow, with fathers and siblings acoustically signalling to embryos directly, rather than through maternal influences (Mariette, 2019; Mariette et al., 2021). Lastly and importantly, except for abnormal acoustic stimuli (e.g. noise, sound deprivation), natural sounds provide information without concurrently altering the suitability of an embryo’s direct environment. For example, heat-calls can inform embryos about heat without changing the temperature that they concurrently experience (Mariette and Buchanan, 2016). The developmental effects of the information received are therefore not confounded with those of developing at suboptimal temperatures. This differs, for example, from low nutrient levels, which may inform embryos on food availability, but also inevitably make their developmental conditions suboptimal, which can lead to a compromised phenotype (Bateson et al., 2004). This is important because the inherent coupling in biochemical cues of information content with developmental condition suitability may hinder our ability to detect adaptive developmental plasticity, when the negative consequences of suboptimal conditions override those of matching the phenotype to current conditions (meta-analysis: Uller et al., 2013). Overall, these properties of acoustic signals, together with the ease of manipulating embryonic acoustic experience (especially in oviparous taxa), open exciting research opportunities for the field of adaptive developmental plasticity in general.

The diversity of immediate and delayed effects of sound on development (Table 1) reveals the intricate – and often unsuspected – interactions between embryos and the external environment (Mariette, 2019; Mariette et al., 2021). This nonetheless suggests that embryos, and developmental processes, may be more susceptible to external disruption than generally assumed. Notably, exposure to anthropogenic noise appears to reduce embryonic development or even survival (Nedelec et al., 2017; Potvin and MacDougall-Shackleton, 2015), and the number of studies across taxa reporting reproductive failure in noisy environments is alarmingly increasing (Kleist et al., 2018; Senzaki et al., 2020). However, parents and their offspring are nearly always concurrently exposed to noise, in both observational (Kleist et al., 2018; Senzaki et al., 2020) and experimental studies (Meillère et al., 2015; Nedelec et al., 2017; Potvin and MacDougall-Shackleton, 2015). It is therefore not known whether detrimental effects on young only occur indirectly through parental disturbance and the disruption of parental care and/or maternal effects (e.g. Liu et al., 2022; Nedelec et al., 2017), or whether noise itself can directly impair development. Loud noise, including during development, is known to cause ‘acoustic trauma’, i.e. damage to hearing organs or other biological structures, from the strength of the mechanical displacement (Kraus and Canlon, 2012; Sole et al., 2018). However, whether chronic moderate noise levels – such as those experienced by humans and wildlife in urban or roadside environments – could directly interfere with developmental processes was unclear until very recently. We (Meillère et al., 2024) showed that exposure to moderate noise prenatally or postnatally directly impairs development and long-term fitness in an altricial bird. These direct effects of noise soundwaves, added to the documented effects of loud noise on the auditory system and other brain areas (see below), are concerning, given the increasing distribution of anthropogenic noise (Buxton et al., 2017). It is thus urgent that we understand the role of natural sounds in developmental processes and the consequences of its disruption.

Understanding acoustic developmental plasticity nonetheless requires identification of the biological or biophysical mechanisms through which sound could alter development. While these mechanisms mostly remain to be established, by bringing together evidence from multiple disciplines, we can identify plausible mechanisms to direct future research. It is likely that at least some mechanisms are shared across taxonomic groups (see below). Birds, and to a lesser extent amphibians, have been most studied, in part because oviparous taxa are most informative, as embryos can be directly exposed to sound without also exposing the mother. Nonetheless, in addition to providing taxonomic breadth, drawing from research on mammals can be insightful, given recent breakthroughs in medical sciences.

Besides specific acoustic cues providing information about current conditions, an embryo’s normal environment includes a diversity of abiotic and biotic sounds (from conspecifics and heterospecifics). This natural soundscape may provide a necessary input for normal auditory development to occur, even though variability is usually not observed (Fig. 2). Only experimental – or anthropogenic – disturbance of that natural soundscape can uncover the role of sound in trait plasticity and development, as nicely illustrated by a series of experiments by Gottlieb in the 1970s and 1980s (reviewed in Gottlieb, 2002). Auditory cues, such as species-specific maternal calls, are more important than visual cues for imprinting in precocial birds (measured by hatchling propensity to follow a decoy mother: Gottlieb, 1968b). Even though naive duck and chicken hatchlings incubated in silence (in artificial incubators) strongly prefer the maternal call of their own species over heterospecific female calls (Gottlieb, 1965), species call recognition is not entirely innate. Fascinatingly, maternal call recognition post-hatch requires prior acoustic input from the embryo's own calls, even though they differ acoustically from maternal calls. Devocalising the embryos, and incubating them alone, leads to ducklings having no preference for the species maternal call (Gottlieb, 1975, 1985, 2002). Further experiments showed that hearing (high-frequency) embryonic calls prenatally is required specifically for perceiving the higher frequency component of maternal calls (Gottlieb, 1975). Furthermore, prenatal exposure to a range of calling rates typical of variable embryonic calls (2–6 calls s−1), as opposed to a constant calling rate, is needed for the preference for maternal call rhythm (at 4 calls s−1) to develop (Gottlieb, 1985, 2002). In agreement with the occurrence of sensitive periods for acoustic developmental programming (Mariette, 2020), the timing of auditory input was also crucial. While a single day of exposure prenatally was sufficient (Gottlieb, 2002), exposure to embryonic calls only postnatally failed to restore the natural preference for species-specific maternal calls (Gottlieb, 1985).

Fig. 2.

Plasticity of auditory sensitivity. Acoustic stimuli from a diversity of sources that normally always occur in the environment (left-hand side) are necessary for the normal development of the auditory centres and their sensitivity to species-specific sounds. Noise can nonetheless interfere with this developmental programming of the auditory system. Hormones, potentially from maternal origin, also plastically modulate auditory sensitivity, by intracellular mechanisms or binding to extracellular receptors. There is ample evidence for such hormone-induced plasticity in adulthood and data suggesting it may also occur in embryos. GC, glucocorticoids; E2, oestrogen; T, testosterone; TH, thyroid hormones.

Fig. 2.

Plasticity of auditory sensitivity. Acoustic stimuli from a diversity of sources that normally always occur in the environment (left-hand side) are necessary for the normal development of the auditory centres and their sensitivity to species-specific sounds. Noise can nonetheless interfere with this developmental programming of the auditory system. Hormones, potentially from maternal origin, also plastically modulate auditory sensitivity, by intracellular mechanisms or binding to extracellular receptors. There is ample evidence for such hormone-induced plasticity in adulthood and data suggesting it may also occur in embryos. GC, glucocorticoids; E2, oestrogen; T, testosterone; TH, thyroid hormones.

Matching behavioural observations, changes also occurred in the auditory system itself, with deprivation from embryonic own calls reducing neuronal activity in the auditory brainstem in duck embryos and hatchlings (Dmitrieva and Gottlieb, 1992). Exposure to prenatal music also had a stimulating effect in chickens: music improved species-specific maternal call preference post-hatch, and increased markers of synaptogenesis in brainstem and forebrain auditory nuclei in embryos and hatchlings, compared with unstimulated individuals (Alladi et al., 2002; Roy et al., 2014). In mammals, moderate noise exposure in rat pups impairs auditory sensitivity and maturation (Chang and Merzenich, 2003). Likewise, in human preterm neonates, exposure to playback of maternal voice and heart beat resulted in a larger auditory cortex than in neonates only exposed to hospital background noise (Webb et al., 2015). Across taxa, exposure to sounds with particular acoustic features and sufficient variability, within a specific sensitive period in prenatal life, therefore appears to be necessary for the normal maturation of the auditory system, and the development of species-specific auditory sensitivity. Beyond sound perception, sound processing and interpretation in the brain may also be partly programmed in early life. Notably, interesting studies on international adoptees, who were only exposed to a native language prenatally and perinatally (until ∼6 months) but never learnt to understand or speak it, suggest that some (subconscious) sound processing mechanisms are retained until late childhood or even adulthood. Brain imagery or performance in linguistic learning tasks revealed a memory for sound processing principles used in their early native language, but absent in the adoption language they learnt postnatally (Choi et al., 2017; Pierce et al., 2014).

Overall, the impact of early acoustic experience goes well beyond the associative learning of prenatal calls, and nicely demonstrates how embedded plasticity is into developmental processes. Nonetheless, it is noteworthy that the source of the acoustic stimuli required for the auditory system maturation should make these plastic, but essential, developmental processes robust to disruption. For example, relying on an embryo's own calls in oviparous species, or maternal sounds in viviparous species, provides robustness, as these cues cannot be absent during normal development. This echoes similar principles of developmental robustness in spite of plasticity for other traits (Hamdoun and Epel, 2007), but also points to possible unforeseen impacts of environmental disruption (such as noise pollution, masking natural sounds), if developmental plasticity occurs in many other as yet undiscovered traits.

In addition to sound, the hormonal environment can also shape auditory development and sensitivity (Fig. 2). In particular, thyroid hormones, which are essential for neuronal differentiation, growth and myelination (Bernal, 2002), as well as for determining the window of sensibility for imprinting (Yamaguchi et al., 2012), may play a particularly important orchestrating role on the development of the auditory pathway, by coordinating the maturation of peripheral and central auditory nuclei (reviewed in Ng et al., 2013). In addition, the cochlea is known to harbour a high density of receptors for both glucocorticoids (GC) and oestrogens in mammals, birds and anurans (Caras, 2013; Charitidi et al., 2012; Kraus and Canlon, 2012; Maney and Pinaud, 2011; Noirot et al., 2009). Accordingly, there is evidence that circulating levels of these hormones at adulthood may modulate auditory sensitivity. For example, in rats, corticosterone can have a protective effect against acoustic trauma caused by loud noise in adulthood (Kraus and Canlon, 2012; Tahera et al., 2007), whereas prenatal stress (mimicked pharmacologically with a GC receptor agonist) increased susceptibility to acoustic trauma later in life (Canlon et al., 2003). Furthermore, oestrogen levels, in the blood stream or the brain, have been found to increase auditory sensitivity across taxa, including humans (Caras, 2013; Coleman et al., 1994; Maney and Pinaud, 2011). Such plasticity can have ecological functions. For example, in midshipman fish (Porichthys notatus), only reproductive females can hear high-frequency male calls, because high oestrogen or testosterone levels (as normally occur in breeding females) are required for the female inner ear to be sensitive to high-frequency sounds (Sisneros et al., 2004). Similarly, in songbirds, androgen levels in the brain are now well known for regulating sexual behaviours, including singing (reviewed in Ball et al., 2020; Maney and Pinaud, 2011) as well as song discrimination in both females (for high-quality songs: Vyas et al., 2008) and males (for the tutor's song or own song: Remage-Healey et al., 2010; Tremere and Pinaud, 2011). In humans and other mammals, prenatal androgen levels might contribute to higher auditory acuity in females (Caras, 2013). Indeed, GC and oestrogen receptors are present very early in embryonic development (e.g. in 37 h old zebra finch embryos: Lutyk et al., 2017), and GC receptors in the auditory system appear to be functional during prenatal life in rats (Canlon et al., 2003). Collectively, these effects offer a mechanistic route for maternally derived hormones to influence embryonic hearing sensitivity, potentially modulating learning of prenatal sounds and/or acoustic developmental programming. Accordingly, experimentally increased testosterone levels in ovo facilitated prenatal auditory learning in bobwhite quail (Bertin et al., 2009), although elevated progesterone levels suppressed learning (Herrington et al., 2015).

Nonetheless, it is important to note that, with the exception of chickens and humans (Hepper and Shahidullah, 1994; Jones et al., 2006), embryonic hearing capacity has rarely been investigated (but see Rivera et al., 2019). Whereas, based on postnatal electrophysiological evidence (e.g. Brittan-Powell and Dooling, 2004), altricial embryos have often been assumed to not hear, the sensitivity of their developmental trajectory to particular prenatal sounds and noise implies otherwise (Mariette et al., 2021). It is unknown whether maternal hormones could temporarily improve embryonic auditory capacity, above that measured postnatally when GC and androgen levels are low (as a result of hypo-responsivity or immaturity of endogenous hormone regulation). It is also unclear whether embryos sense the airborne sounds, or instead the associated vibratory cues. Sound and vibrations are the same physical phenomenon of a displacement of particles through a medium. When sound is produced, for example, by a bird singing in a tree, a signal with the same frequency and temporal characteristics travels as sound in the air and as vibration in any solid that the emitter touches (i.e. the tree; Caldwell, 2014). With their head against the eggshell, avian embryos are thought to perceive sounds by bone transmission (Rumpf and Tzschentke, 2010), although this remains to be tested. Further studies on prenatal auditory ontogeny and its plasticity are needed to unravel the full capacity (and susceptibility) of embryos across taxa.

While an impact of nutrients, hormones, chemicals and even temperature on development makes intuitive sense, the possibility that sound could also alter developmental processes is more surprising. Yet, similar to changes in the auditory system, sound could have a broader impact in the brain – and therefore development – if the auditory pathway projects onto key controlling brain regions. Indeed, accumulated evidence in neurobiology clearly indicates that the auditory pathway in the brain is connected to several other brain regions not directly implicated in sound perception (Durand et al., 1992; Hoke et al., 2005; Janak and Tye, 2015; Kraus and Canlon, 2012; Nabavi et al., 2014; Rogan et al., 1997). Three of these brain regions – namely, the hippocampus, amygdala and hypothalamus – belong to the limbic system, and are well-known targets of developmental programming (Banerjee et al., 2012; Lupien, 2009; Welberg and Seckl, 2001). Their connectivity with auditory nuclei may therefore provide the necessary basis for acoustic stimuli to trigger broad organismal effects, in adults or young, but also points specifically to a possible role of sound in developmental programming.

Evidence for auditory connectivity to different brain regions comes from studies in mammals (mostly humans and rodent models) and/or birds and anurans. Importantly, nonetheless, the auditory pathway (nuclei and projections) shows striking homology between mammals and birds (and anurans at least for sub-cortical areas: Jarvis, 2004). Further, the hypothalamus, hippocampus and to some degree the amygdala are homologous in mammals, birds and anurans, based on shared developmental origin, function, neurochemistry (including neuron types) and connectivity, allowing some meaningful comparisons (Jarvis et al., 2005; Moreno and Gonzalez, 2007; O'Connell and Hofmann, 2011; note the avian nomenclature was revised in 2004). The evidence for the auditory sensitivity of these limbic regions also comes from several different approaches, only some of which have been used in embryos. Specifically, neuro-anatomical studies, and the great majority of studies on functional connectivity, showing immediate responses triggered by sound [evidenced, for example, by functional magnetic resonance imaging (fMRI) or immediate early genes (IEGs); see Glossary], have only been conducted in mature individuals (e.g. Koelsch, 2014; Wild, 2017). By contrast, studies on developing young and embryos have mostly investigated delayed effects of acoustic experience, including those on neurogenesis or neuronal degeneration in the limbic regions (e.g. Chaudhury et al., 2006; de Almeida et al., 2020). These delayed responses suggest that some anatomical and functional connections were present during development, although this was not directly tested. Below, while not aiming at an exhaustive review, I synthesise what we know to date about the auditory connectivity of the hippocampus, amygdala and hypothalamus (Fig. 3), and how these connections could, in principle, allow sound-triggered developmental plasticity in an ecological context.

Fig. 3.

Schematic representation of the auditory pathway in the avian brain and its connection to key limbic regions for developmental programming: the hippocampus, amygdaloid complex and hypothalamus. The auditory pathway (in blue) ascends from the hair cells in the cochlea to the cochlear nuclei (CN) and lateral lemniscal nuclei (LL) in the brainstem (which together with the cerebellum makes the hindbrain), the mesencephalicus lateralis pars dorsalis (Mld) nucleus (or inferior colliculus in mammals) in the midbrain, the ovoidalis nucleus (Ov; media geniculate in mammals) in the thalamus, and finally the field L complex (L1–L3), projecting to the caudal part of the medial nidopallium (NCM) and the caudal part of the medial mesopallium (CMM) (avian homologue to the mammalian auditory association cortex). Projections (in orange) to limbic areas (in red) occur from several auditory nuclei along the pathway. The connections to the hippocampus (Hipp) are only indirect (dashed line), presumably starting from the NCM. The ovoidalis nucleus in the thalamus directly projects onto the amygdaloid complex (Amyg; or specifically the nucleus taeniae, which, with the arcopallium, makes the avian amygdaloid complex; the same connection occurs in mammals onto the basolateral amygdala). Note the placement of the amygdala can vary between bird orders (e.g. columbiform versus passeriform: Cheng et al., 1999). Lastly, the connection to the hypothalamus (Hypo) from the thalamic nucleus is direct in birds (and anurans), but not mammals. For simplicity, back connections from higher to lower auditory nuclei are not shown, nor are reciprocal connections from limbic areas to the auditory pathway. SO, superior olive; CLM, caudolateral mesopallium. Illustration by Lou Laizé Mariette.

Fig. 3.

Schematic representation of the auditory pathway in the avian brain and its connection to key limbic regions for developmental programming: the hippocampus, amygdaloid complex and hypothalamus. The auditory pathway (in blue) ascends from the hair cells in the cochlea to the cochlear nuclei (CN) and lateral lemniscal nuclei (LL) in the brainstem (which together with the cerebellum makes the hindbrain), the mesencephalicus lateralis pars dorsalis (Mld) nucleus (or inferior colliculus in mammals) in the midbrain, the ovoidalis nucleus (Ov; media geniculate in mammals) in the thalamus, and finally the field L complex (L1–L3), projecting to the caudal part of the medial nidopallium (NCM) and the caudal part of the medial mesopallium (CMM) (avian homologue to the mammalian auditory association cortex). Projections (in orange) to limbic areas (in red) occur from several auditory nuclei along the pathway. The connections to the hippocampus (Hipp) are only indirect (dashed line), presumably starting from the NCM. The ovoidalis nucleus in the thalamus directly projects onto the amygdaloid complex (Amyg; or specifically the nucleus taeniae, which, with the arcopallium, makes the avian amygdaloid complex; the same connection occurs in mammals onto the basolateral amygdala). Note the placement of the amygdala can vary between bird orders (e.g. columbiform versus passeriform: Cheng et al., 1999). Lastly, the connection to the hypothalamus (Hypo) from the thalamic nucleus is direct in birds (and anurans), but not mammals. For simplicity, back connections from higher to lower auditory nuclei are not shown, nor are reciprocal connections from limbic areas to the auditory pathway. SO, superior olive; CLM, caudolateral mesopallium. Illustration by Lou Laizé Mariette.

Hippocampus

At its origin in the 1970s–1980s, prenatal acoustic communication was mostly investigated in the context of imprinting and associative learning, in precocial birds and humans (Decasper and Fifer, 1980; Gottlieb, 2002). As the hippocampus is involved in memory and spatial learning (Kraus and Canlon, 2012; Krebs et al., 1989; Morris et al., 1982), this is the (non-auditory) brain region that has received by far the most attention regarding its responsivity to prenatal sounds. Nonetheless, the anatomical connectivity with the auditory pathway is not as straightforward as for other regions. In mammals, the hippocampus receives auditory input via direct and indirect connections from auditory association cortices, rather than from the subcortical auditory pathway (Koelsch, 2014; Kraus and Canlon, 2012). The connectivity in birds is much less clear (Bailey and Saldanha, 2015).

Functional connectivity, nonetheless, has been demonstrated repeatedly in both taxonomic groups. In human adults, a meta-analysis of fMRI studies showed that music, and specifically musical novelty, reliably triggers neuronal activity in the hippocampus (Koelsch, 2014), while in other mammals the hippocampus responds, for example, to distress calls (but not similar tones) (in rats: Ouda et al., 2016) and to some echolocation calls (in bats: Yu and Moss, 2022). In songbirds (but not doves: Terpstra et al., 2005), several IEG studies have demonstrated that the hippocampus responds specifically to species-specific songs or calls, in both adults (Bailey et al., 2002; Bolhuis et al., 2000; Gobes et al., 2009; Vignal et al., 2008) and juveniles (Bailey and Wade, 2003, 2005). However, this response varies with sex (sometimes stronger in females: Bailey and Saldanha, 2015; Gobes et al., 2009; Vignal et al., 2008), context (Kruse et al., 2004; Maney et al., 2008) or even the emitter's social status (mate versus non-mate: Vignal et al., 2008). This may explain variation between studies, but also implies some level of sound processing prior to the hippocampal response.

Furthermore, there is evidence that acoustic experience in early life, including prenatally, triggers delayed changes in the hippocampus in both mammals and birds. For example, in rats, while maternal grooming deprivation famously reprogrammes the offspring hippocampus and stress axis (Liu et al., 1997; Weaver et al., 2004), playback of maternal calls to pups during separation from the mother is sufficient to prevent these deleterious changes in the brain (Ziabreva et al., 2003). Furthermore, music exposure from birth to adulthood (3 months old) improved rat spatial cognition and, in the hippocampus, increased the density of the synthetic neurogenesis marker bromodeoxyuridine (BrdU; see Glossary), and the expression of brain-derived neurotrophic factor (BDNF; see Glossary) and its receptor (TrkB), involved in neuronal growth and brain plasticity (Xing et al., 2016). By contrast, retrograde music, in which the notes were reversed to disrupt the rhythm while preserving other properties of the music (again played from birth to 3 months), had the opposite effect on learning and the hippocampus (Xing et al., 2016). Similar effects occurred with sound experienced prenatally, with music and loud noise exposure respectively enhancing or reducing BrdU density in 3 week old rat pups (Kim et al., 2006). Beyond the maternal-care provisioning period, loud noise exposure, although only experienced for 2 weeks post-weaning, reduced rat hippocampal neurogenesis (BrdU) at adulthood (Jauregui-Huerta et al., 2011). Likewise, in chickens, prenatal exposure to music enhances hippocampal size, and both prenatal music and species-specific calls increase BDNF levels, and other markers of neurogenesis and associated molecular and synaptic activity in the hippocampus (Chaudhury et al., 2006, 2008; Chaudhury and Wadhwa, 2009), whereas loud prenatal noise exposure has the opposite effect (Sanyal et al., 2013). These effects of prenatal experience in birds are visible at hatching (Chaudhury et al., 2006; Chaudhury and Wadhwa, 2009; Sanyal et al., 2013), or even during embryonic development (Chaudhury et al., 2008; Chaudhury and Wadhwa, 2009). However, whether, as in mammals, they persist at maturity has not been tested. As in rats, sound-triggered changes in the avian hippocampus are paralleled by differences in learning performance at hatching, although effects vary slightly across studies (Chaudhury et al., 2010; Kauser et al., 2011; Sanyal et al., 2013).

Overall, these studies demonstrate that acoustic experience during development induces plasticity in a brain area important for learning and cognition, which could have some carry-over effects later in life. In mammals, maternal physiological responses to sound could have confounded effects of prenatal or pre-weaning exposure. Yet, the similarity of these effects to those observed for exposures after weaning in rats, or prenatally in birds (incubated artificially), suggests instead a possible direct embryonic response to sound even in mammals. The presence of similar responses in mammals and birds is also consistent with these effects being possibly widespread, but non-model species are yet to be investigated.

Amygdala

In birds and mammals, the amygdala also plays a major role in memory, and is the main central regulator of ‘emotions’, motivation and reward behaviour, as well as being implicated in social behaviours (Janak and Tye, 2015; McGaugh, 2002; McGaugh et al., 1996; O'Connell and Hofmann, 2011). Despite a less straightforward taxonomic homology (Jarvis et al., 2005; O'Connell and Hofmann, 2011), responses to sound in the mammalian amygdala and avian ‘amygdaloid complex’ are similar. In mammals, the amygdala is particularly responsive to vocalisations, music and sound features with an emotional valence (e.g. alarm calls, rising intensity sound, music: Bach et al., 2008; Gil-Da-Costa et al., 2004; Koelsch, 2014; Ouda et al., 2016; Sander et al., 2003). Even human newborns showed a different response in the amygdala (and auditory cortex) to normal versus dissonant music (Perani et al., 2010). Less is known about the particular acoustic features that the avian amygdaloid complex responds to, but specific activation by songs (rather than tones: Maney et al., 2008) or arrhythmic songs (rather than normal songs) has been documented in adult birds (Lampen et al., 2014; but see Lampen et al., 2017).

Remarkably, in both mammals and birds, particular neurons in the amygdala are fine-tuned to particular biologically relevant sounds: different species-specific vocalisations selectively activate distinct populations of amygdaloid neurons in adult bats (Gadziola et al., 2016) and songbirds (Fujii et al., 2016). Indeed, there are direct anatomical connections from the ascending auditory pathway to the amygdala in both groups. Namely, the auditory nucleus in the thalamus directly projects onto the amygdala in mammals (Nabavi et al., 2014; Rogan et al., 1997; reviewed in: Janak and Tye, 2015; Kraus and Canlon, 2012), birds (including columbiform and passeriform: Cheng et al., 1999; Fujii et al., 2016) and anurans (Hall et al., 2013); while another direct projection from the cortical auditory nucleus has also been described in mammals (Janak and Tye, 2015; Kraus and Canlon, 2012). Most fascinatingly, the direct connection from the thalamic auditory nucleus to the amygdala is well known for underlying the classic Pavlovian conditioning response in adult mammals, whereby individuals learn to respond physiologically to a sound presented just prior to a threat or reward (Janak and Tye, 2015; Nabavi et al., 2014; Rogan et al., 1997; Tye et al., 2008). This learnt response solely occurs because of the strengthening of the synaptic connection from the thalamic auditory nucleus to the amygdala. The strength of this synapse matches the individual's learning score (Tye et al., 2008), and learning can be induced or reversed by manipulating this synapse by optogenetic stimulation (Nabavi et al., 2014).

This sound-induced plasticity, which is to date the most unequivocal physical trace of memory, demonstrates the powerful influence of acoustic experience on behaviour and physiology. It also represents a very promising avenue for developmental programming, if prenatal sounds could trigger similar effects. For example, we may hypothesise that, given the role of the amygdala in motivation, reward and social behaviour (Janak and Tye, 2015; McGaugh, 2002; McGaugh et al., 1996; O'Connell and Hofmann, 2011), amygdaloid plasticity could potentially underlie the impact of prenatal acoustic experience on nestling begging intensity in semi-precocial and altricial birds (Mariette and Buchanan, 2016; Noguera and Velando, 2019a), or imprinting on prenatal calls in precocial birds (e.g. Bertin et al., 2009; Lickliter, 1990). Indeed, the amygdala is known to develop early during embryonic development, including in songbirds (present in late-stage embryos: Ikebuchi et al., 2013; Mayer et al., 2019; Vicario et al., 2017). Given that the sound-induced amygdaloid plasticity relies on simple changes in synapse strength, and only involves sub-cortical brain areas, it could, in principle, occur early in development, potentially before the sound-processing regions in the cortex develop. Nonetheless, to date, to the best of my knowledge, the effects of prenatal sounds on the amygdala have only been investigated in humans. In preterm neonates, exposure to music is able to counter the negative impact of a noisy hospital environment on amygdala size (de Almeida et al., 2020).

Hypothalamus

The hypothalamus orchestrates the body's endocrine and metabolic response to the environment, by sitting atop three key regulatory axes, namely the (i) hypothalamic–pituitary–adrenal (HPA; see Glossary) axis, regulating the release into the blood stream of glucocorticoid (cortisol or corticosterone) and noradrenaline, involved in the stress response and metabolic regulation, as well as hatching (Banerjee et al., 2012; Lupien, 2009; Romero, 2004; Sapolsky et al., 2000; Tong et al., 2013; Welberg and Seckl, 2001); (ii) the hypothalamic–pituitary–thyroid (HPT; see Glossary) axis, releasing thyroid hormones, which control metabolism, thermogenesis, growth, hatching and, importantly, brain development (Debonne et al., 2008; Hsu et al., 2017; McNabb, 2007; Ng et al., 2013; Tong et al., 2013); and (iii) the hypothalamic–pituitary–gonadal (HPG; see Glossary) axis, controlling the release of steroid hormones, which at least in the case of avian maternal hormones (e.g. testosterone and androstenedione), are known to influence nestling begging and growth, or even sexual behaviour at adulthood (Groothuis, 2019; Groothuis and Schwabl, 2008; Muriel et al., 2015; Partecke and Schwabl, 2008). The hypothalamus is itself also regulated by the hippocampus and the amygdala (Moreno and Gonzalez, 2007; O'Connell and Hofmann, 2011; Smulders, 2017). It is well known that the HPA axis in particular is shaped by early-life conditions and maternal hormones, with long-lasting consequences on the individual phenotype, in both humans/rodents (Liu et al., 1997; Lupien, 2009; Welberg and Seckl, 2001) and birds (Banerjee et al., 2012; Groothuis, 2019; Groothuis and Schwabl, 2008).

In mammals, there is no direct connection from auditory nuclei to the hypothalamus (Janak and Tye, 2015; Kraus and Canlon, 2012), but network analyses in adult humans indicated that music can trigger activity in the hypothalamus via the amygdala (Koelsch and Skouras, 2014). By contrast, early tracing studies in amphibians (Allison and Wilczynski, 1991; Neary and Wilczynski, 1986), doves (Cheng and Zuo, 1994; Durand et al., 1992) and more recently songbirds (Wild, 2017; Zeng et al., 2004) have identified clear direct connections from the thalamic and midbrain auditory nuclei to the hypothalamus. Several studies in anurans have also reported the excitatory effect of species calls on the hypothalamus neuronal activity (Allison, 1992; Hoke et al., 2005; Wilczynski and Allison, 1989). For example, in tungara frogs (Physalaemus pustulosus), playback of male calls increased the expression of the IEG egr-1 in females' auditory and hypothalamic area (Hoke et al., 2005). While the hypothalamic regions activating upon sound stimulation did not vary across stimuli (heterospecific calls, or intact or modified conspecific calls), the subsequent pattern of activation within the hypothalamus did differ (Hoke et al., 2005). As for the amygdala, meaningful acoustic information can thus be encoded in the hypothalamus and specifically alter its activity. Similarly, in birds, a landmark study on auditory reproductive activation in female ring doves (Cheng et al., 1998) demonstrated that natural coo calls (but not modified calls) trigger a specific response in hypothalamic neurons, which stimulated luteinising hormone (LH) release from the pituitary. Male and female coo calls triggered a similar level of hypothalamic activity, but the LH release was 3 times greater in response to female calls (Cheng et al., 1998), again suggesting a response of the hypothalamic axis tuned to the biological relevance of the sound. Whether such a level of specificity occurs in early development in currently unknown. A hypothalamic IEG response to calls (versus silence) has been detected at hatching in quails (chickens not tested), but in both species, differential responses to conspecific versus heterospecific calls were only detectable overall across brain regions, and not specifically in the hypothalamus (or any other region considered singly; Long et al., 2002).

Further to immediate hypothalamic responses during sound exposure, there is some evidence for longer-term effects. For example, in adult mice, music exposure for 3 weeks increased BDNF levels in the hypothalamus (although nerve growth factor levels decreased; Angelucci et al., 2007). Furthermore, in adult green-tree frogs, chorus call exposure increased the number of hypothalamic gonadotropin-releasing hormone (GnRH)-producing neurons in males, with downstream increases in testosterone, dihydrotestosterone and corticosterone levels (Burmeister and Wilczynski, 2000, 2005). Without measuring hypothalamic responses per se, similar changes in downstream androgen or corticosterone levels in response to vocalisations have also been demonstrated in adult birds (Moser-Purdy et al., 2017; Wikelski et al., 1999), but also in altricial nestlings (Tilgar et al., 2010), or following loud noise exposure in rat pups (Jauregui-Huerta et al., 2011). Prenatally, although not consistently, exposure to maternal calls, music or loud noise can lead to differences in corticosterone or noradrenaline in chicken hatchlings (Kauser et al., 2011; Sanyal et al., 2013), and, in gulls, prenatal alarm call exposure may increase corticosterone levels in hatchlings (Noguera and Velando, 2019a,b). These effects on hormone levels suggest, although do not demonstrate, changes in the hypothalamus prenatally. Likewise, prenatal exposure to music increased the growth of particular hypothalamic neurons in rat pups (Russo et al., 2021), but these effects may be confounded by maternal exposure.

The onset of acoustic developmental programming responses during ontogeny is contingent on the embryo's ability to first receive the vibro-acoustic signal, through some means of perception (Mariette, 2020). That animals possess a specialised organ (e.g. cochlea) and neural circuitry to perceive sounds does not preclude the existence of other perception pathways. For example, red-eyed treefrog (Agalychnis callidryas) embryos have sophisticated vibration-sensing capacities through their vestibular system (Warkentin, 2005). Yet, they can also detect vibrations with movement-sensing neuromast cells, which mature before vestibular sensitivity, thereby bringing forward the age at which embryos can start detecting predators (Jung et al., 2020). During vertebrate ontogeny, movement and then vibration sensing develops, before hearing, and then vision (Gottlieb, 1968a). Based on eco-devo principles, immature embryos may rely on more primitive senses to detect sounds and vibrations. Fascinatingly, many earless and brainless organisms are responsive to sound (Fig. 4), including fish and mollusc larvae (Simpson et al., 2005; Sole et al., 2018), or even plants and unicellular organisms (Aggio et al., 2012; Gagliano, 2013; Gagliano et al., 2012; Mishra et al., 2016).

Fig. 4.

Examples of brainless and earless organisms known to be affected by sound. (A) Arabidopsis thaliana is used widely in plant research: seedlings orientate their roots towards sound, and sound alters gene expression and phytohormone levels. (B) Pea seedlings orientate their roots towards the vibro-acoustic cues of water running in a pipe. (C,D) Loud noise damages the gravity-sensing cells (statocysts) in the roots of the seagrass Posidonia oceanica (C), as well damaging sensory cells in three cephalopod species, with hatchlings showing higher susceptibility than adults (D). (E) Sound increases growth rate in baker's yeast culture and alters metabolite composition. (F) Fish larvae (e.g. damselfish) use sound to locate coral reefs for settlement.

Fig. 4.

Examples of brainless and earless organisms known to be affected by sound. (A) Arabidopsis thaliana is used widely in plant research: seedlings orientate their roots towards sound, and sound alters gene expression and phytohormone levels. (B) Pea seedlings orientate their roots towards the vibro-acoustic cues of water running in a pipe. (C,D) Loud noise damages the gravity-sensing cells (statocysts) in the roots of the seagrass Posidonia oceanica (C), as well damaging sensory cells in three cephalopod species, with hatchlings showing higher susceptibility than adults (D). (E) Sound increases growth rate in baker's yeast culture and alters metabolite composition. (F) Fish larvae (e.g. damselfish) use sound to locate coral reefs for settlement.

While plant acoustics initially met with some scepticism (ten Cate, 2013; but see Khait et al., 2023), there is now no doubt that at least some plants are sensitive to sound and/or vibrations, even if the mechanisms of perception and actuation are still under investigation (reviewed in Demey et al., 2023; Mishra et al., 2016; Teixeira da Silva and Dobranszki, 2014). Notably, many plants require vibro-acoustic stimulation from an insect pollinator to release their pollen: the insect vibrates in a stereotyped body position on the plant anther, which opens the anther pores. Such ‘buzz pollination’ occurs in 65 plant families, and many bee species, with the buzz having particular acoustic characteristics (De Luca and Vallejo-Marin, 2013). Furthermore, some plants are instead sensitive to sound from herbivorous insects, which triggers chemical defences in the plant (Appel and Cocroft, 2014; Demey et al., 2023; Pinto et al., 2019). Remarkably, as in embryos, one study suggests anticipatory effects: the vibrations from a chewing caterpillar had no immediate effect, but induced higher chemical defences later on, when the plant was actually attacked by caterpillars (Appel and Cocroft, 2014). This response was specifically tuned to ecologically relevant cues, as vibrations from wind or non-herbivorous stimuli (leafhopper song) had no effect (Appel and Cocroft, 2014). In addition, abiotic sounds, such as running water, may provide important information to plants, including during development. Following an inspiring preliminary observation in corn seedlings (Gagliano et al., 2012), roots of Arabidopsis seedlings have been shown to strongly orientate towards sound (of 200 Hz) versus silence (Rodrigo-Moreno et al., 2017), and roots of pea seedlings have been found to grow towards the vibrations produced by running water, without any humidity cues to rely on (Gagliano et al., 2017). Agronomical research has also investigated sound effects on plant development using artificial sounds (pure tones), although the ecological function of these effects is unknown. A few studies suggest that germination and growth may be improved by sounds of particular frequencies (Collins and Foreman, 2001; Creath and Schwartz, 2004; Teixeira da Silva and Dobranszki, 2014; Wang et al., 2002), although an indication of sample sizes and replication across multiple growth chambers would be critical. By contrast, noise may, as in animals, decrease plant growth and increase oxidative stress (Kafash et al., 2022), and loud noise can even cause physical damage to marine plants (Sole et al., 2021).

Furthermore, there are reports of sound modulating growth in unicellular organisms such as yeast or Escherichia coli, or even potentially in plant cell cultures (reviewed in: Demey et al., 2023; Mishra et al., 2016; Teixeira da Silva and Dobranszki, 2014). Fascinatingly, animal cell cultures – including precursor and embryonic cells – also directly responded to audible sound (Kumeta et al., 2018). Such effects, if corroborated, could potentially allow direct cellular sensing of vibrations in living embryos. While the field of cellular acoustic sensitivity is still in its infancy, exciting recent breakthroughs in medical sciences (Rufo et al., 2022), such as music-sensitive transgenic cells delivering insulin to treat diabetes (Zhao et al., 2023), raise the possibility of a so-far unforeseen mode of sound perception. The 2021 Nobel Prize in Physiology or Medicine was attributed to Ardem Patapoutian for discovering pressure- or sound-sensitive ion channels in vertebrate cell membranes (Kefauver et al., 2020; Latorre and Diaz-Franulicb, 2022). Some of these mechanosensitive channels (e.g. ‘Piezo1’, TRAAK) respond to ultrasounds, with the acoustic mechanical force tensing the cell membrane and specifically opening the channel (Rufo et al., 2022; Sorum et al., 2021). While medical sciences mostly uses high ultrasounds, some ultrasound-sensitive genes appear responsive to audible sounds (Kumeta et al., 2018). Particular sounds could thus directly act on cells, by triggering cascades of intracellular mechanisms from the influx of particular ions, including Ca2+ and K+, known for their cellular signalling functions (Luan and Wang, 2021). Interestingly, in plants, blocking Ca2+ cytoplasmic influx pharmacologically prevents the growth-enhancing or root-attraction effect of sound (Rodrigo-Moreno et al., 2017; Wang et al., 2002). Based on sound-evoked cellular responses, several pathways downstream of Ca2+ influx have been proposed, which may eventually alter gene expression (Demey et al., 2023; Ghosh et al., 2016; Mishra et al., 2016; Rodrigo-Moreno et al., 2017; Teixeira da Silva and Dobranszki, 2014).

There are also some interesting parallels between plants and animals at the organismal level, which deserve further investigation. Notably, there is evidence that several phytohormones, which regulate cell division, may be involved in sound-induced plant growth (Demey et al., 2023; Ghosh et al., 2016; Kafash et al., 2022; Mishra et al., 2016). Furthermore, acoustic stimulation increases the production of reactive oxygen species (ROS; see Glossary) and anti-oxidant enzymes in plants (Demey et al., 2023; Kafash et al., 2022; Mishra et al., 2016; Rodrigo-Moreno et al., 2017). In animals, acoustic trauma involves increases in ROS (Kraus and Canlon, 2012), and the deleterious effect of noise or alarm calls on telomere length during development suggests heightened oxidative damage (Meillère et al., 2015; Noguera and Velando, 2019b). One plant study also reported changes to ATP production (Yang et al., 2003), while in zebra finch nestlings, prenatal sounds shape mitochondrial efficiency (Udino et al., 2021). Together, whilst preliminary, these observations raise the possibility for sound to produce organismal effects as observed in developing animals, in the absence of a (mature) brain, or even potentially through direct cellular responses.

The multi-disciplinary evidence reviewed here shows that, beyond the subtle refinement of auditory centre maturation by acoustic and endocrine stimuli, the brain is specifically wired to allow acoustic impact on physiology. The mere presence of anatomical connections from the auditory pathway to key limbic regions, and the fine-tuning of that functional connectivity to the biological meaning of the sounds, demonstrate the fascinating capacity for sound to plastically modulate the brain. This connectivity allows many physiological and behavioural changes in the individual, without requiring any sound processing or interpretation by the cortex. Furthermore, the brain is designed in such a way that, once received, the acoustic information can programme development through exactly the same pathways as the (extensively studied) maternal hormones (Mariette et al., 2021). While the evidence during early development is still very limited, investigating the programming of the brain by sound represents a very promising avenue for future research.

Determining the timing of development of the auditory pathway (Hepper and Shahidullah, 1994; Jones et al., 2006), the limbic regions (Debonne et al., 2008; Ikebuchi et al., 2013; Tong et al., 2013) and crucially their connectivity is an important next step, in both altricial and precocial species. Nonetheless, the window of sensitivity to acoustic programming of different limbic regions may differ depending on their timing of maturation and whether they receive input from sub-cortical or cortical auditory nuclei. In addition, for anticipatory cues, it is expected that changes in the brain would predate downstream effects, which may only be manifested postnatally when the organism needs to respond to the environmental conditions predicted by the prenatal sound. For example, sound-induced changes in the hypothalamus (e.g. through epigenetic markers) could occur during its maturation prenatally (Lupien, 2009), but only have organismal effects later on, when the hypothalamus starts regulating endocrine secretions. This may be analogous to the organisational–activational principle of sex steroids, differentiating brain development prenatally, and only later activating behavioural differences at sexual maturity (Arnold, 2009; Phoenix et al., 1959).

That the connectivity of limbic regions to the auditory pathway is broadly conserved across amphibians, birds and mammals suggests that sound-induced plasticity is widespread, rather than rare. This connectivity may be a conserved ancestral trait or have evolved multiple times across lineages. In either case, its broad taxonomic occurrence suggests not only that such connectivity serves a purpose but also that sound-induced plasticity probably brings significant fitness advantages (e.g. Mariette and Buchanan, 2016; Warkentin, 2005).

Overall, in the same way that elucidating the mechanisms of maternal allocation and embryonic uptake is starting to illuminate the many documented effects of maternal hormones (Groothuis, 2019; Groothuis and Schwabl, 2008), uncovering the mechanisms of acoustic development programming will bring biological realism to the nonetheless unequivocal evidence that sound is capable of altering development. While we are far from identifying a universal response to sound, spontaneous effects of sound and vibrations across the living kingdom, including on brainless and unicellular organisms, are consistent with the hypothesis that embryos, even with immature senses, are able to respond to prenatal sounds. Recent progress in medicine suggests that we may be at the dawn of a new era, where the full impact of ultrasounds, audible sounds and vibrations on living organisms is unravelled.

I thank two anonymous reviewers for their useful comments.

Funding

This work was supported by the Ministerio de Ciencia, Inovacion y Universidades (grants RYC2019-028066-I and PID2021-128494NA-100) and the Australian Research Council (grants DE170100824 and DP210101238).

Special Issue

This article is part of the Special Issue ‘Developmental plasticity: from mechanisms to evolutionary processes’, guest edited by Patricia A. Wright and Kathleen M. Gilmour. See related articles at https://journals.biologists.com/jeb/issue/227/Suppl_1.

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Competing interests

The author declares no competing or financial interests.