Abstract
The place theory proposed by Jeffress (1948) is still the dominant model of how the brain represents the movement of sensory stimuli between sensory receptors. According to the place theory, delays in signalling between neurons, dependent on the distances between them, compensate for time differences in the stimulation of sensory receptors. Hence the location of neurons, activated by the coincident arrival of multiple signals, reports the stimulus movement velocity. Despite its generality, most evidence for the place theory has been provided by studies of the auditory system of auditory specialists like the barn owl, but in the study of mammalian auditory systems the evidence is inconclusive. We ask to what extent the somatosensory systems of tactile specialists like rats and mice use distance dependent delays between neurons to compute the motion of tactile stimuli between the facial whiskers (or ‘vibrissae’). We present a model in which synaptic inputs evoked by whisker deflections arrive at neurons in layer 2/3 (L2/3) somatosensory ‘barrel’ cortex at different times. The timing of synaptic inputs to each neuron depends on its location relative to sources of input in layer 4 (L4) that represent stimulation of each whisker. Constrained by the geometry and timing of projections from L4 to L2/3, the model can account for a range of experimentally measured responses to two-whisker stimuli. Consistent with that data, responses of model neurons located between the barrels to paired stimulation of two whiskers are greater than the sum of the responses to either whisker input alone. The model predicts that for neurons located closer to either barrel these supralinear responses are tuned for longer inter-whisker stimulation intervals, yielding a topographic map for the inter-whisker deflection interval across the surface of L2/3. This map constitutes a neural place code for the relative timing of sensory stimuli.
Highlights
A fundamental question in computational neuroscience asks how the brain represents the relative timing of stimuli as they move between sensory receptors, e.g. as a light source moves relative to the retina, or as contact moves between touch sensors on the fingertip
To perceive how stimuli move over sensor surfaces like the retina or the fingertips, neurons in the brain must report the relative timing of signals arriving at different locations on the sensor surface
These results suggest a link between the location of the neuron and the relative timing of sensory signals reported by its activity
Summary
A fundamental question in computational neuroscience asks how the brain represents the relative timing of stimuli as they move between sensory receptors, e.g. as a light source moves relative to the retina, or as contact moves between touch sensors on the fingertip. The inter-sensor time difference is encoded by the location of neurons that are active because their connection delays exactly compensate the inter-sensor stimulation interval. The place theory suggests an important role for neural geometry in computing the motion of sensory stimuli. Strong support for Jeffress’ place theory has been provided by a number of studies of midbrain neurons in auditory specialists like the barn owl, who locate sound sources by resolving small differences in the arrival time of sounds at either ear Evidence from the mammalian auditory system is less conclusive because, for example, rabbit auditory cortex neurons are tuned to inter-ear time differences that are too long to attribute to inter-neuron distances alone [3] Few studies have investigated how intersensor time-differences might be resolved in specialist mammalian sensory systems
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