Our senses tell us what is around us, informing us of approaching danger, nearby mates and sources of food. The intensity of these stimuli varies, and in order to cope with this, our senses adapt: in the dark our eyes are keener than in daylight, and in a quiet room our sense of hearing is more sensitive than out in the street. At a cellular level, this process ensures that the same number of action potentials is fired in response to stimuli of different intensities by the neurons that process the sensory information. While adaptation serves to enhance our ability to detect important things around us, the brain loses information on the absolute value of stimuli. However, for some tasks this information is critical. How can the nervous system deal with these seemingly contradictory demands?
In a paper recently published in PLoS Biology, a team from universities in Oldenburg, Berlin, and Tuebingen, Germany, shed light on this process by looking at auditory communication in grasshoppers. A male grasshopper, as it tries to identify the call of a potential mate, should adapt its hearing to deal with the varying intensity of the auditory stimulus, but, at the same time, can only detect her location by comparing the difference in intensity of the call between his two ears (the closer ear will hear a slightly louder call). To tackle this problem, the team first had to see where in the nervous system adaptation occurs.
The team performed recordings of neurons within the ear and the local neurons to which they talk as the grasshopper's ears transduce sound information to local neurons. These neurons in turn relay the information to two separate channels going up into the central brain: a channel for the sound pattern (which encodes the identity of the sound, and benefits from adaptation) and another for the difference in intensity between the ears – the ‘location channel’ – which encodes location, and suffers from adaptation. The team found that, by the time the sound information has reached the local neurons, it has been perfectly adapted: they fire the same number of spikes in response to sounds of different intensities. Crucially, this adaptation takes around 50 ms, which means that within that initial time window the local neurons still have information on the intensity of the sound: the more intense the stimulus, the more action potentials these cells fire. The cells in the location channel could potentially read out the information collected in the first 50 ms in order to detect the location of the call.
To test this hypothesis, the team recorded from one such neuron, AN2, to see its response to an acoustic stimulus. They noticed that AN2 only fires action potentials during the first 50 ms of the stimulus, actively shutting itself off after that time. This suggests that this location neuron is tuned to the process of adaptation within the ear and the local neurons, responding to when the information encodes the location of the call, and ignoring it when it encodes the call identity, which would only confuse it.
This work therefore shows how the nervous system's changing response to a stimulus over time can overcome the problem of both having to remove a source of sensory information and depending on it for a behavioural task, a principle that could apply to sensory processing in all animals (such as you and me).