Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system

Abstract

Sensory perception involves the dual challenge of encoding external stimuli and managing the influence of changes in body position that alter the sensory field. To examine mechanisms used to integrate sensory signals elicited by both external stimuli and motor activity, we recorded from rats trained to rhythmically sweep their vibrissa in search of a target. We found a select population of neurons in primary somatosensory cortex that are transiently excited by the confluence of touch by a single vibrissa and the phase of vibrissa motion in the whisk cycle; different units have different preferred phases. This conditional response enables the rodent to estimate object position in a coordinate frame that is normalized to the trajectory of the motor output, as defined by phase in the whisk cycle, rather than angle of the vibrissa relative to the face. The underlying computation is consistent with gating by an inhibitory shunt.The perception of object location relative to the body depends on tracking sensor positioneyes for seeing or fingers for touching-as much as on the activation of those sensors by features of an object. Over a half century ago, von Holst 1 emphasized that one cannot hope to understand sensation without consideration of the effects "produced on the sensoryreceptors by the motor impulses which initiate a muscular movement." von Holst factored the signals required for sensation into three components. One is an afferent signal that originates from environmental influences-for example, light for the case of looking and pressure for the case of touching-and is denoted ex-afference. A second component is an afferent signal that results from activation of sensory receptors by self-motion and is called reafference. The motor-driven sensory input can involve the same receptors that encode external stimuli, as in the case of peripheral reafference, or a separate group of receptors, as in the case of proprioception. A final sensory component may be provided by an efference copy of the motor command; this corresponds to the intended rather than actual motor activation of sensory receptors. The ex-afferent component can interact with one or both motor signals (that is, reafference or efference copy) to produce a perceptually stable representation of the identity and location of external stimuli relative to a changing body configuration. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptThe coexistence and possible interaction of ex-afference, reafference and efference copy signals has been demonstrated from peripheral to thalamocortical levels 2 . In gaze control, reafferent signals of actual eye position and efference copy of the intended position of gaze3 gate the input to vestibular nuclei as part of the vestibular ocular response4. In the visual system, neurons in cat thalamus5 and primary visual cortex 6 respond to visual stimuli (the ex-afferent signal) and to the stimulation of extra-ocular muscle proprioceptors (a reafferent signal). Further, interactions between ex-af...

Radial distance determination in the rat vibrissal system and the effects of Weber's law

“…This identity-based coding scheme is consistent with the central neural representation of vibrissae in a manner that reflects the regular topographical arrangement of vibrissae on the face [12,13]. The manner in which the rat's nervous system codes information about horizontal angular contact position (u) and radial object distance (r) is more problematic, as there are no proprioceptors in the muscles that control the vibrissae to provide information about u [1,14], and there are no sensors along the length of the vibrissae to provide information about r [15,16]. Previous publications have described some possible coding mechanisms for u [1,3,14,16 -18].…”

Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons

“…Indeed, time-varying second-order attributes occur in natural stimuli in the form of low-frequency envelopes and often contain behaviorally relevant information (Ahissar et al, 2000;Joris et al, 2004;Curtis and Kleinfeld, 2009). Our results suggest a general strategy for designing brain circuits that selectively extract envelope information.…”

Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex

“…Behaviour vectors were constructed as follows. Owing to the relatively slow kinetic properties of YC-Nano140 and the low image acquisition rate (7 Hz) compared to observed whisking frequency (8 to 12 Hz) 13,14,20,38 , measured calcium signals are unlikely to reflect whisking frequency accurately or to distinguish slow changes in whisking amplitude from fast rhythmic variation in position 15,20 . As rhythmic and non-rhythmic whisking occurred (Supplementary Video 3), whisking amplitude was used as a measure to represent both forms of whisking behaviour.…”

“…Responses in S1 were sparse, with 34% of L2/3 neurons showing activity during the behaviour session. S1 neurons are responsive to both whisker motion during free whisking 13,14 and sensory input from whisker touch [15][16][17] . Our image acquisition rate was too low to observe locking of neuronal responses with rhythmic whisking 15 or surface palpitations 9 , so for a simple functional classification we cross-correlated cellular calcium signals across all trials against the envelope of whisking amplitude and a binary vector representing touch periods, respectively (Fig.…”

“…Cross correlation was performed on each sub-vector and the overall correlation to whisker angle was obtained by taking the maximum R value across the eight sub-vectors. Owing to limited imaging speed, slow calcium-indicator kinetics, and because L2/3 neuronal activity in S1 is largely devoid of fast touch signals 15,16 , measured calcium responses are not likely to represent instantaneous kinematic features. The correlation values obtained represent relative measures of response preferences to these parameters solely to permit a comparison across cell types.…”