The neural basis of the behaviorally relevant N1 component of the somatosensory-evoked potential in SI cortex of awake monkeys: evidence that backward cortical projections signal conscious touch sensation

Abstract

Studies of touch intensity discrimination in monkeys have identified a component of the somatosensory-evoked cortical potential, N1, generated within 50 ms of the stimulus, that predicts their behavioral performance. This study employed multiple-electrode arrays with relatively high spatial resolution (0.1 or 0.2 mm spacing) to record laminar profiles of somatosensory-evoked potentials (SEPs), multiple unit activity (MUA) and current source-densities (CSDs) at several sites across the postcentral gyri of two awake monkeys. This high resolution laminar analysis strongly supports our earlier hypothesis based upon low resolution data that N1 is generated by synaptic excitation targeted specifically at the most superficial cortical layers I/II: (1) The excitatory nature of N1 was indicated by elevated MUA which was maximal in layer III and extended down to subcortical white matter where fiber activity exceeded prestimulus levels; (2) In addition to CSD analysis, the observation that N1 was maximally negative within 0.10 mm of the border between layers I and II verified the superficial site of N1 synaptic excitation regardless of conductivity boundaries near the pial surface. A review of the anatomical literature finds that the most likely inputs responsible for N1 activation are the "backward" cortico-cortical projections from secondary somatosensory areas to SI which in area 1 are the major source of sensory-related input that specifically terminates in layers I/II. We suggest, therefore, that backward projections are involved in the conscious process of touch sensation as it is signaled by N1.

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

“…Importantly, there is substantial evidence to suggest that top-down processes not only play an important role in sensory processing in general but also are crucial for conscious perception, in particular [75][76][77][78][79][80][81][82] (see also the review articles by Pollen, 83 Lamme and Roelfsema, 84 Bullier, 85 Hochstein and Ahissar, 86 and Meyer 87 ). For example, when subjects perceive apparent motion (as is the case when two dots in different locations are seen in rapid alteration, creating the impression that a single dot is moving from one location to the other), there is V1 activity along the apparent motion trace (where there is no actual visual stimulus), and this activity is induced by top-down signals.…”

“…77 Similar findings exist for the somatosensory modality: the subjective intensity of tactile stimuli is reflected in top-down signals that reach layer 1 of the primary somatosensory cortex from higher-level areas rather than in the thalamocortical signals that initially arrive in layer 4. 75,76 As an additional observation, which applies equally to the visual, auditory, and somatosensory modalities, there is an interdependency of the latency of sensory cortex responses and their correlation with conscious experience: although early activity in the sensory areas appears to be strictly stimulus bound, later activity, which reflects top-down signals from higher-order cortices, is correlated more closely with the subject's conscious percept. 24,75,76,79,89,90 Thus, several lines of evidence from neuroanatomy, neurophysiology, and functional neuroimaging suggest that top-down signaling fulfills an indispensable function in conscious perception.…”

“…75,76 As an additional observation, which applies equally to the visual, auditory, and somatosensory modalities, there is an interdependency of the latency of sensory cortex responses and their correlation with conscious experience: although early activity in the sensory areas appears to be strictly stimulus bound, later activity, which reflects top-down signals from higher-order cortices, is correlated more closely with the subject's conscious percept. 24,75,76,79,89,90 Thus, several lines of evidence from neuroanatomy, neurophysiology, and functional neuroimaging suggest that top-down signaling fulfills an indispensable function in conscious perception. Accordingly, if general anesthetics interrupt top-down processing, as suggested by the studies reviewed at the outset of the article, this would be one potential mechanism by virtue of which they may suspend consciousness.…”

Coupling between somatosensory evoked potentials and hemodynamic response in the rat

“…The origin of P1 from SI-specific thalamocortical inputs is well established (Mitzdorf, 1985). N1 is associated with the slow, long latency sink in layers I/II (Agmon and Connors, 1991;Kulics and Cauller, 1986) and is generated by excitatory cortical events (Cauller and Kulics, 1991). N1 is reduced during deep anesthesia (Arezzo et al, 1981) and slow-wave sleep (Cauller and Kulics, 1988).…”

Enhanced dendritic activity in awake rats

“…One leading hypothesis is that during awake sensory processing, thalamo-cortical interactions involving deep-layer pyramidal neurons result in non-specific thalamic nuclei projecting feedback input to the tuft dendrites of L5 pyramidal neurons (4). It is also hypothesized that higher cortical areas (more active during conscious processing) project to the same tuft dendrites in L1 in primary sensory areas (5,6). Both these hypotheses predict specific input to pyramidal cell dendrites during the awake state.…”