Receptive fields and response properties of neurons in the star-nosed mole's somatosensory fovea

Star-nosed moles have an extraordinary mechanosensory system consisting of 22 densely innervated nasal appendages covered with thousands of sensitive touch domes. A single appendage acts as the fovea and the star is constantly shifted to touch this foveal appendage to objects of interest. Here we investigated the receptive fields on the star and the response properties of 144 neurons in the mole's primary somatosensory cortex (S1). Excitatory receptive fields were defined by recording multiunit activity from the S1 representations of the nasal appendages that form the star, while stimulating the touch domes on the skin surface with a small probe. Receptive fields were among the smallest reported for mammalian glabrous skin, averaging <1 mm(2). The smallest receptive fields were found for the fovea representation, corresponding to its greater cortical magnification. Single units were then isolated, primarily from the representation of the somatosensory fovea, and the skin surface was stimulated with a small probe attached to a piezoelectric wafer controlled by a computer interface. The response properties of neurons and the locations of inhibitory surrounds were evaluated with two complementary approaches. In the first set of experiments, single microelectrodes were used to isolate unit activity in S1, and data were collected for stimulation to different areas of the sensory star. In the second set of experiments, a multi-electrode array (4 electrodes spaced at 200 microm in a linear sequence) was used to simultaneously record from isolated units in different cortical areas representing different parts of the sensory periphery. These experiments revealed a short-latency excitatory discharge to stimulation of the fovea followed by a long-lasting suppression of spontaneous activity. Sixty-one percent of neurons responded with an excitatory OFF response at the end of the stimulus; the remaining 39% of cells did not respond or were inhibited at stimulus offset. Stimulation of areas surrounding the central receptive field often revealed inhibitory surrounds. Forty percent of the neurons that responded to mechanosensory stimulation of the receptive field center were inhibited by stimulation of surrounding areas of skin on the same appendage. In contrast to neurons in rodent barrels, few neurons within a stripe representing an appendage responded to stimulation of neighboring (nonprimary) appendages on the snout. The small receptive fields, short latencies, and inhibitory surrounds are consistent with the star's role in rapidly determining the locations and identities of objects in a complex tactile environment.