Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons

Abstract

1. Localized cortical cooling was employed in anesthetized cats for the rapid reversible inactivation of the distal forelimb region within the primary somatosensory cortex (SI). The aim was to examine the responsiveness of individual neurons in the second somatosensory area (SII) in association with SI inactivation to evaluate the relative importance for tactile processing of the direct thalamocortical projection to SII and the indirect projection from the thalamus to SII via an intracortical path through SI. 2. Response features were examined quantitatively before, during, and after SI inactivation for 29 SII neurons, the tactile receptive fields of which were on the glabrous or hairy skin of the distal forelimb. Controlled mechanical stimuli that consisted of l-s trains of either sinusoidal vibration or rectangular pulses were delivered to the skin by means of small circular probes (4- to 8-mm diam). 3. Twenty-three of the 29 SII neurons (80%) showed no change in response level (in impulses per second) as a result of SI inactivation. These included seven neurons activated exclusively or predominantly by Pacinian corpuscle (PC) receptors, six that received hair follicle input, four activated by convergent input from hairy and glabrous skin, and six driven by dynamically sensitive but non-PC inputs from the glabrous skin. 4. Six SII neurons (20%), also made up of different functional classes, displayed a reduction in response to cutaneous stimuli when SI was inactivated. 5. Stimulus-response relations, constructed by plotting response level in impulses per second against the amplitude of the mechanical stimulus, showed that the effect of SI inactivation on individual neurons was consistent over the whole response range. 6. The reduced response level seen in 20% of SII neurons in association with SI inactivation cannot be attributed to direct spread of cooling from SI to the forelimb area of SII, as there was no evidence for a cooling-induced prolongation in SII spike waveforms, an effect that is known to precede any cooling-induced reduction in responsiveness. 7. As SI inactivation produced a fall in spontaneous activity in the affected SII neurons, we suggest that the inactivation removes a source of background facilitatory influence that arises in SI and affects a small proportion of SII neurons. 8. Phase-locking and therefore the precision of impulse patterning were unchanged in the responses of SII neurons to vibration during SI inactivation. This was the case whether response levels of neurons were reduced or unchanged by SI inactivation.(ABSTRACT TRUNCATED AT 400 WORDS)

Interaction between afferent input from fingers in human somatosensory cortex

“…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.…”

Parallel Processing of Nociceptive and Non-nociceptive Somatosensory Information in the Human Primary and Secondary Somatosensory Cortices: Evidence from Dynamic Causal Modeling of Functional Magnetic Resonance Imaging Data

“…Indeed, an alternative interpretation could be that the functional state of S2 is dependent on the functional state of S1, through intrinsic connections between the two areas [i.e., S1 could exert a control on the excitability of S2 neurons (Turman et al, 1992)]. Hence, the ablation of S1 could reduce the responsiveness of S2 to non-nociceptive inputs originating directly from the thalamus, by removing a background facilitatory influence of S1 on the neural activity in S2 (Turman et al, 1992). Our results, suggesting a direct processing of non-nociceptive somatosensory input from the thalamus to S2 (Fig.…”

“…In lower primates, several studies have shown that nonnociceptive somatosensory information is transmitted from the thalamus to both S1 and S2 via segregated thalamocortical pathways, thus indicating a parallel processing of non-nociceptive somatosensory input in S1 and S2 (Garraghty et al, 1991;Turman et al, 1992). In contrast, the processing of non-nociceptive somatosensory input in higher primates and humans remains, at present, a matter of debate Iwamura, 1998).…”

Processing of Vibrotactile Inputs From Hairy Skin by Neurons of the Dorsal Column Nuclei in the Cat

“…From here, the information is conveyed over a parallel projection network to two principal cerebral cortical target regions, the primary and secondary somatosensory areas of the cortex (SI and SII, respectively) (Bennett et al 1980;Ferrington and Rowe 1980b;Fisher et al 1983;Mackie et al 1996;Rowe et al 1985;Turman et al 1992Turman et al , 1995Zhang et al 1996Zhang et al , 2001a. At the cortical level, a substantial decline is apparent in SI, in the tightness of phaselocking of individual responses, with phaselocking absent at vibration frequencies above ϳ100 Hz (Ferrington and Rowe 1980b;Mountcastle et al 1969), whereas within SII, individual neurons can retain phaselocked responses at vibration frequencies up to ϳ300 Hz (Ferrington and Rowe 1980b;Ghosh et al 1992;Rowe 1990;Rowe et al 1985).…”