1. 1.

    The tibial campaniform sensilla are a group of mechanoreceptors in the cockroach leg that respond to cuticular strain. Each sensillum consists of a single bipolar neurone whose dendrite inserts into an ovoid cuticular cap embedded in the exoskeleton.

  2. 2.

    The tibial campaniform sensilla are consistently separable into two subgroups with mutually perpendicular cap orientation: the long axis of the caps of proximal subgroups are oriented perpendicular to the tibial long axis; caps of the distal subgroup are parallel to the tibia.

  3. 3.

    The responses of individual, identified sensilla from both subgroups were tested to the following forces: bending forces (perpendicular to the leg long axis), axial forces (parallel to the leg axis), torques (twisting about the leg long axis) and forces generated by the tibial muscles.

  4. 4.

    The tibial campaniform sensilla respond vigorously to bending forces imposed in the plane of movement of the adjacent femorotibial joint. Individual sensilla exhibit orientation-dependent directional sensitivity in their response: the proximal sensilla respond only to dorsal bending; the distal sensilla respond only to ventral bending. Sensilla respond less vigorously to bending forces in other planes.

  5. 5.

    Responses are weak but directionally sensitive to axial forces: the proximal sensilla fire upon axial compression; the distal sensilla fire upon axial tension.

  6. 6.

    Both subgroups respond simultaneously but weakly to imposed torques.

  7. 7.

    Contractions of the tibial muscles produce strong orientation dependent responses: the proximal sensilla respond only to flexor muscle contractions; the distal sensilla respond only to extensor muscle contractions.

  8. 8.

    These responses are accurately predicted from a simple model in which the tibia behaves as a cylinder under stress. The tibial campaniform sensilla respond as directionally sensitive strain gauges. Each individual sensillum responds only to compressions perpendicular to the long axis of its cuticular cap.

  9. 9.

    Tibial campaniform sensilla respond best to those forces that the animal can most effectively control.

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