Bilateral Integration of Whisker Information in the Primary Somatosensory Cortex of Rats

Abstract

The isomorphic representation of the contralateral whisker pad in the rodent cerebral cortex has served as a canonical example in primary somatosensory areas that the contralateral body surface is spatially represented as a topographic map. By characterizing responses evoked by multiwhisker stimuli, we provide direct evidence that the whisker region of the rat primary somatosensory cortex (SI) integrates information from both contralateral and ipsilateral whisker pads. The proportions of SI neurons responsive to ipsilateral whisker stimuli, as well as their response probabilities, increased with the number of ipsilateral whiskers stimulated. Under bilateral whisker stimulation, the responses of 95% of neurons recorded were affected by stimulation of ipsilateral whiskers. Contralateral tactile responses of SI neurons were profoundly influenced by preceding ipsilateral stimuli and vice versa. This effect depended on both the spatial location and the relative timing of bilateral whisker stimuli, leading to both spatial and temporal asymmetries of interaction. Bilateral whisker stimulation resulted in only modest changes in evoked response latency. Previous ipsilateral stimulation was also shown to affect tactile responses evoked by later ipsilateral stimuli. Inactivation of the opposite SI abolished ipsilaterally evoked responses as well as their influence on subsequently evoked contralateral responses in the intact SI. Based on these results, we conclude that the rat SI integrates information from both whisker pads and propose that such interactions may underlie the ability of rats to discriminate bilateral tactile stimuli. Key words: barrel cortex; bilateral; ipsilateral; integration; interhemispheric transfer; inactivation; topographyThe role of the somatosensory cortex (SI) in integrating separate sources of tactile input has been investigated primarily by inferring from extracellular recordings the spatiotemporal transformations performed on convergent subcortical inputs. The whisker region of the SI in rodents is an ideal model for investigating the issue of cortical integration because of its modular topography, which purportedly reflects the arrangement of contralateral whiskers at the periphery (Woolsey and Van der Loos, 1970;Killackey, 1973). Recordings from SI neurons in temporal interaction studies have provided a basic description of the temporal and spatial attributes of cortical integration elicited by paired contralateral whisker stimuli (Simons, 1985;Simons and Carvell, 1989;Brumberg et al., 1996;Fanselow and Nicolelis, 1999). Such studies suggest that the SI may integrate information across multiple contralateral whiskers to generate behaviorally relevant information regarding the animal's surrounding environment.If the rat is to use tactile information from both sides of its face, left and right whisker information must also be integrated. Comparisons between these separate sources of tactile input would then allow the animal to successfully detect the width of an aperture, or the orientation of ...

Ipsilateral Whiskers Suppress Experience-Dependent Plasticity in the Barrel Cortex

“…In the rodent, it has been observed that deflection of ipsilateral whiskers suppresses cortical responses evoked by contralateral whisker stimulation (Shuler et al, 2001), consistent with other anatomical (Carr and Sesack, 1998) and electrophysiological (Kawaguchi, 1992) evidence supporting the conclusion that, under normal conditions, callosal inputs have a net inhibitory influence.…”

“…Although transection of the corpus callosum, the main anatomical structure that connects the two cortical hemispheres, results in only subtle sensory and motor deficits (Gazzaniga, 2000), many studies have confirmed that cortical neuron responses can be strongly influenced by activation of peripheral ipsilateral inputs (Armstrong-James and George, 1988;Clarey et al, 1996;Shuler et al, 2001Shuler et al, , 2002Pluto et al, 2005).…”

“…The clear anatomy of the rodent somatosensory cortex, where individual whiskers project to topographically defined cortical columns (Woolsey and Van der Loos, 1970), as well as the complete crossing of primary sensory afferents at the midline (Waite, 1969;Smith, 1973;Erzurumlu and Killackey, 1980), makes this an attractive system to study the influence of interhemispheric interactions in shaping receptive field properties (Clarey et al, 1996;Shuler et al, 2001Shuler et al, , 2002Pluto et al, 2005). In the rodent, it has been observed that deflection of ipsilateral whiskers suppresses cortical responses evoked by contralateral whisker stimulation (Shuler et al, 2001), consistent with other anatomical (Carr and Sesack, 1998) and electrophysiological (Kawaguchi, 1992) evidence supporting the conclusion that, under normal conditions, callosal inputs have a net inhibitory influence.…”

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

“…The SII fields are connected by callosal fibers, and their role may not be simply combining excitatory signals of two hemispheres to yield bilateral receptive fields. Experiments using denervation or reversible inactivation have attributed transcallosal activity a modulatory role in bilateral interactions (Shuler et al, 2001). In addition to the direct callosal projection, SII and SI fields in the two hemispheres can also interact via fibers descending to the thalamus (Raij et al, 2008).…”

“…Interhemispheric connections between the barrel fields were described by Olavarria et al (1984) and Koralek et al (1990) in the rat, who found that they are confined to the septal regions. The work on unanesthetized rats by Shuler et al (2001) and Wiest et al (2010) found a proportion of units that responded to stimulation of vibrissae from either side of the muzzle in layer V of the barrel cortex. Bilateral subthreshold receptive fields were also described in that layer by Manns et al (2004).…”