Physiological Evidence for Serial Processing in Somatosensory Cortex

Pons, T. P.; Garraghty, Preston E.; Friedman, D. P.; Mishkin, Mortimer

doi:10.1126/science.3603028

Cited by 238 publications

(140 citation statements)

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“…Based on this line of evidence, and in addition to the welldescribed thalamic ventral posterior complex (VP) projecting densely to S1 Powell, 1969b, 1970;Burton and Jones, 1976;Lin et al, 1979), a hierarchical scheme of somatosensory transmission pattern was constructed, in which peripheral information is processed sequentially from VP thalamus to S1 and then to S2. This hypothesis was supported further by lesion studies, that is, removal of an S1 representation abolished the somatic evoked response in the corresponding S2 region in macaques and rhesus monkeys (Pons et al, 1987(Pons et al, , 1988Burton et al, 1990). In contrast, S1 responsiveness was not affected by the elimination of the homotypical S2 region (Pons et al, 1988).…”

supporting

confidence: 65%

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

Liao

Yen

2008

The Anatomical Record

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The hierarchical relationship of the rat primary somatosensory cortex (S1) and secondary somatosensory cortex (S2) is controversial. The existence of a direct thalamocortical projection from ventral posterolateral thalamic nucleus (VPL) to S2 is a key factor in determining the relative position of S2 in the processing flow. In this study, the inter-connections of forepaw and hindpaw representations in VPL, S1, and S2 were examined by neuroanatomical tracing and electrophysiological approaches. In the tracing experiments, VPL, S1, and S2 were electrophysiologically identified, and then iontophoretically injected with biotinylated dextran amine (BDA, a bi-directional tracer). In the double-labeling experiments, two of the following retrograde tracers-BDA, Rhodamine dextran (RD), and/or Fluoro-Gold (FG)-were injected into homotypical S1 and S2 forepaw representations simultaneously. In the electrophysiological studies, paired somatic evoked multiunit responses in S1 and S2 were compared. Our results revealed that: (1) VPL forepaw and hindpaw neurons projected to corresponding S1 and S2 areas in a parallel and somatotopic manner; (2) very low percentage of double projecting VPL neurons were found, indicating parallel and independent pathways from forepaw VPL to S1 and S2; (3) forepaw S1 and S2 were symmetrically and reciprocally connected; (4) response latencies of the S1 and S2 multiunits to forepaw stimulation were in accordance with a direct and parallel pathway. This study provides further evidence to support the equivalent hierarchy of S1 and S2 in processing sensory information of the rat. Anat Rec, 291:960-973, 2008. 2008 Wiley-Liss, Inc.Key words: parallel; primary somatosensory cortex; serial; ventral posterolateral thalamic nucleusThe peripheral somatosensory information is known to convey to the contralateral primary somatosensory cortex (S1) and secondary somatosensory cortex (S2).Although extensive studies have been carried out on the thalamocortical and corticothalamic circuitry of the somatosensory system, whether S1 and S2 process Abbreviations used: Ang 5 angular thalamic nucleus; BDA 5 biotinylated dextran amine; CPu 5 caudate putamen; eml 5 external medullary lamina; ic 5 internal capsule; ml 5 medial lemniscus; POm 5 posterior medial nucleus; RD 5 rhodamine dextran; Rt 5 reticular thalamic nucleus; str 5 superior thalamic radiation; VA 5 ventroanterior thalamic nucleus; VL 5 ventrolateral thalamic nucleus; VM 5 ventromedial thalamic nucleus; VPL 5 ventral posterolateral thalamic nucleus; VPM 5 ventral posteromedial thalamic nucleus; ZId 5 zona incerta, dorsal part.

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supporting

confidence: 65%

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

Liao

Yen

2008

The Anatomical Record

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“…Deactivation of SI in cats or prosimian primates had no notable effect on the responsiveness of SII neurons to cutaneous stimuli [9,14,26]. Nevertheless, ablations of SI, and even areas 3a and 3b alone, totally deactivated the SII area in monkeys, implying serial processing of the somatic information [15,28]. However, recent studies by Turman et al [32] and Rowe et al (1994, personal communication) suggest that tactile input can reach SII directly from thalamus both in cats and in monkeys, and that SI may have a backround facilitatory influence on the function of SII.…”

Section: Discussionmentioning

confidence: 99%

Interaction between afferent input from fingers in human somatosensory cortex

Forss¹,

Jousmäki²,

Hari³

1995

Brain Research

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We recorded somatosensory evoked magnetic fields from eight healthy subjects with a 122-channel whole-scalp SQUID magnetometer. The stimulus sequence consisted of 'standard' stimuli (85%) delivered to palmar side of the left thumb with an interstimulus interval of 0.6 s and of 'deviants' (15%), randomly interspersed among the standards, to little finger, and vice versa. Both stimuli activated four source areas: the contralateral primary somatosensory cortex (SI), the contra-and ipsilateral secondary somatosensory cortices (SII), and the contralateral posterior parietal cortex (PPC). The short-latency (20-40 ms) responses originated in the SI cortex, whereas long-latency responses arose from all 4 areas. At SII and PPC, the deviant stimuli elicited larger responses when presented alone, without intervening standards, than among standards. This implies interaction between afferent impulses from the two fingers and/or partly intermingled cortical representations. Our findings show, in agreement with animal data, different excitatory/inhibitory balance in the various somatosensory areas.

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“…In this model, neurons that have partially invariant (ID and IC) or strongly locally tuned responses provide feedforward, convergent input to neurons that show invariance across the entire finger pad. Another possibility, which is not mutually exclusive, is that the convergent inputs for all of the tuned SII region neurons come from lower-order somatosensory neurons in SI that project to the SII region (Friedman et al, 1980(Friedman et al, , 1986Pons et al, 1987Pons et al, , 1992Burton et al, 1995;Disbrow et al, 2003). Previous studies have shown that many of the RFs in SI show approximately linear response properties and have approximately circular or slightly elongated lobes of excitation or inhibition, like most of the D, C, and DC neurons we report here (DiCarlo et al, 1998;Sripati et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Receptive Field Properties of the Macaque Second Somatosensory Cortex: Nonlinear Mechanisms Underlying the Representation of Orientation Within a Finger Pad

Thakur¹,

Fitzgerald²,

Lane³

et al. 2006

J. Neurosci.

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We investigate the position invariant receptive field properties of neurons in the macaque second somatosensory (SII) cortical region. Previously we reported that many SII region neurons show orientation tuning in the center of multiple finger pads of the hand and further that the tuning is similar on different pads, which can be interpreted as position invariance. Here we study the receptive field properties of a single finger pad for a subset (n ϭ 61) of those 928 neurons, using a motorized oriented bar that we positioned at multiple locations across the pad. We calculate both vector fields and linear receptive fields of the finger pad to characterize the receptive field properties that give rise to the tuning, and we perform an additional regression analysis to quantify linearity, invariance, or both in individual neurons. We show that orientation tuning of SII region neurons is based on a variety of mechanisms. For some neurons, the tuning is explained by simple excitatory regions, simple inhibitory regions, or some combination of these structures. However, a large fraction of the neurons (n ϭ 20 of 61, 33%) show position invariance that is not explained well by their linear receptive fields. Finding invariance within a finger pad, coupled with the previous result of similar tuning on different pads, indicates that some SII region neurons may exhibit similar tuning throughout large regions of the hand. We hypothesize that invariant neurons play an important role in tactile form recognition.

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Physiological Evidence for Serial Processing in Somatosensory Cortex

Cited by 238 publications

References 19 publications

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

Interaction between afferent input from fingers in human somatosensory cortex

Receptive Field Properties of the Macaque Second Somatosensory Cortex: Nonlinear Mechanisms Underlying the Representation of Orientation Within a Finger Pad

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