Response Properties of Whisker-Related Neurons in Rat Second Somatosensory Cortex

Abstract

Kwegyir-Afful, Ernest E. and Asaf Keller. Response properties of whisker-related neurons in rat second somatosensory cortex. J Neurophysiol 92: 2083-2092. First published May 26, 2004 10.1152/jn.00262.2004. In addition to a primary somatosensory cortex (SI), the cerebral cortex of all mammals contains a second somatosensory area (SII); however, the functions of SII are largely unknown. Our aim was to explore the functions of SII by comparing response properties of whisker-related neurons in this area with their counterparts in the SI. We obtained extracellular unit recordings from narcotized rats, in response to whisker deflections evoked by a piezoelectric device, and compared response properties of SI barrel (layer IV) neurons with those of SII (layers II to VI) neurons. Neurons in both cortical areas have similar response latencies and spontaneous activity levels. However, SI and SII neurons differ in several significant properties. The receptive fields of SII neurons are at least five times as large as those of barrel neurons, and they respond equally strongly to several principal whiskers. The response magnitude of SII neurons is significantly smaller than that of neurons in SI, and SII neurons are more selective for the angle of whisker deflection. Furthermore, whereas in SI fast-spiking (inhibitory) and regularspiking (excitatory) units have different spontaneous and evoked activity levels and differ in their responses to stimulus onset and offset, SII neurons do not show significant differences in these properties. The response properties of SII neurons suggest that they are driven by thalamic inputs that are part of the paralemniscal system. Thus whisker-related inputs are processed in parallel by a lemniscal system involving SI and a paralemniscal system that processes complimentary aspects of somatosensation. I N T R O D U C T I O NThe cerebral cortex of all mammals contains several representations for each sensory modality. For example, there exist upward of 32 morphologically and functionally discrete visual cortical areas in primates (Van Essen et al. 1992). Similarly, in all species, there exist several discrete somatosensory and auditory cortical areas (Disbrow et al. 2003;Harel et al. 2000;Huang and Winer 2000;Welker and Sinha 1972;Woolsey 1967). The roles and relationships of these multiple sensory representations are controversial. In the visual system, there is evidence that different cortical regions process information hierarchically, such that visual information is processed serially from one cortical area to the next (Casagrande and Kaas 1994;Kennedy and Bullier 1985;Stone et al. 1979). However, there is also evidence that visual information is processed in parallel by multiple cortical areas (Herkenham 1980;Weyand and Swadlow 1986). A similar ambiguity characterizes somatosensory cortical regions, with evidence existing for both serial and parallel processing by different cortical areas (Burton 1991;Coleman et al. 1999; Dykes 1983;Pons et al. 1992;Turman et al. 1995;Zhang et al. 1996)....

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

“…The distance between VPL neurons and their S2 destination is shorter than the path taken by VPL-S1 axons. Our result is consistent with several previous studies (Woolsey and Wang, 1945;Heppelmann et al, 2001;Kwegyir-Afful and Keller, 2004), which showed that S1 and S2 neurons responded to peripheral stimulation with similar peak latencies in rabbits and rats. However, Brett-Green et al (2003, 2004 and Benison et al (2007) examined epipial-evoked potentials when stimulating a rat's whisker and other body regions, and found a much longer latency of evoked response in S2 than in S1.…”

“…In the higher-primates, S2 lost the direct thalamic afferents and depend on the corticocortical inputs from ipsilateral S1 for activation. Summing the various aforementioned studies, results favoring serial transmission were performed mostly on macaque and rhesus monkeys (Pons et al, 1987(Pons et al, , 1988(Pons et al, , 1992Burton et al, 1990), while investigations supporting the parallel view used nonprimitive primates and other mammals, including rats, cats, marmoset monkeys, tree shrews, and opossums (Spreafico et al, 1981;Fisher et al, 1983;Murray et al, 1992;Turman et al, 1995;Coleman et al, 1999;Heppelmann et al, 2001;Zhang et al, 2001a,b;Kwegyir-Afful and Keller, 2004). Our results from rats further support the distinction between serial somatosensory processing in higher primates and parallel somatosensory processing in other mammals.…”

“…In the current study, electrical stimulation was applied to the forepaw, while studies by Brett-Green et al (2003, 2004 and Benison et al (2007) used mechanical stimulation. However, Kwegyir-Afful and Keller (2004) examined S1 and S2 responses evoked by whisker deflection, and found that S1 and S2 responded with similar peak latencies. In addition, we investigated the evoked S1 and S2 responses by multiunit recording, whereas Brett-Green et al used epipial-evoked potential.…”

Bilateral Plasticity of Vibrissae SII Representation Induced by Classical Conditioning in Mice

“…In rats, independent inputs to SI and SII were described with anatomical and electrophysiological techniques (Kwegyir-Afful and Keller, 2004), and a direct parallel pathway to SII from VPL was demonstrated (Liao and Yen, 2008). A recent study in mice using flavoprotein autofluorescence imaging in brain slices (Theyel et al, 2010), combined with anatomical and electrophysiological experiments confirmed it.…”

Consistency of Angular Tuning in the Rat Vibrissa System

“…Typically, analysis of angular tuning has been performed only on responses to deflections of the principal vibrissae, which evoke the largest magnitude responses in their associated neurons. However, many vibrissae in a receptive field may evoke spikes, and in some brain regions, these adjacent (nonprincipal) vibrissae can evoke response magnitudes similar to those evoked by the principal vibrissa (principal trigeminal nucleus: Veinante and Deschênes 1999;thalamus: Diamond et al 1992; primary somatosensory cortex: Bruno and Simons 2002; second somatosensory cortex: Kwegyir-Afful and Keller 2004;superior colliculus: Hemelt and Keller 2007). This raises the question whether the angular tuning of the principal vibrissa is preserved across the receptive field, that is, if nonprincipal vibrissae within a receptive field respond with similar angular tuning to those produced by the principal vibrissa.…”