Frequency Adaptation Modulates Spatial Integration of Sensory Responses in the Rat Whisker System

Michael J. Higley, Diego Contreras
2007 Journal of Neurophysiology  
Higley MJ, Contreras D. Frequency adaptation modulates spatial integration of sensory responses in the rat whisker system. The generation of perceptual experiences requires the integration of complex spatiotemporal patterns of sensory input. The rodent whisker system is a useful model for understanding the cellular mechanisms of sensory integration, which often include the operation of local circuits distributed throughout the brain. An example is cross-whisker suppression, where the neuronal
more » ... here the neuronal response to whisker deflection is strongly reduced by preceding deflection of a neighboring whisker. Suppressive interactions between whiskerevoked responses have largely been studied using pairs of single whisker deflections. However, rats typically sweep their whiskers across surfaces at frequencies ranging from 5 to 25 Hz. Repetitive afferent activation induces frequency-dependent adaptation of neuronal responses and alters the synaptic dynamics of circuits that play a role in suppression, suggesting that adaptation could modulate the spatial integration of whisker evoked responses. We tested this hypothesis by comparing the cross-whisker suppression of principal whisker (PW)-evoked cortical and thalamic responses when preceded by either a single deflection of an adjacent whisker (AW) or a train of AW deflections at frequencies covering the normal whisking range. We found that periodic deflection of the preceding AW significantly reduced the magnitude of cross-whisker suppression. Surprisingly, although higher frequencies resulted in greater adaptation of the AW-evoked response, the effect on suppression was independent of frequency. We suggest that these results follow from known local circuit operations at multiple levels within the afferent path. Our findings support the view that repetitive whisking subserves a transformation of the integrative and functional properties of the whisker system. Ahissar E, Sosnik R, Haidarliu S. Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406: 302-306, 2000. Arnold PB, Li CX, Waters RS. Thalamocortical arbors extend beyond single cortical barrels: an in vivo intracellular tracing study in rat. Exp Brain Res 136: 152-168, 2001. Brecht M, Preilowski B, Merzenich MM. Functional architecture of the mystacial vibrissae. Behav Brain Res 84: 81-97, 1997. Carvell GE, Simons DJ. Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638 -2648, 1990. Castro-Alamancos MA. Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J Physiol 539: 567-578, 2002a. Castro-Alamancos MA. Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J Neurophysiol 87: 946 -953, 2002b. Castro-Alamancos MA, Oldford E. Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J Physiol 541: 319 -331, 2002. Chmielowska J, Carvell GE, Simons DJ. Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. Moore CI. Frequency-dependent processing in the vibrissa sensory system. J Neurophysiol 91: 2390 -2399, 2004. Sheth BR, Moore CI, Sur M. Temporal modulation of spatial borders in rat barrel cortex. J Neurophysiol 79: 464 -470, 1998. Simons DJ, Carvell GE. Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61: 311-330, 1989. Timofeeva E, Lavallee P, Arsenault D, Deschenes M. Synthesis of multiwhisker-receptive fields in subcortical stations of the vibrissa system. J Neurophysiol 91: 1510 -1515, 2004. Varga C, Sik A, Lavallee P, Deschenes M. Dendroarchitecture of relay cells in thalamic barreloids: a substrate for cross-whisker modulation. J Neurosci 22: 6186 -6194, 2002. Veinante P, Deschenes M. Single-and multi-whisker channels in the ascending projections from the principal trigeminal nucleus in the rat. J Neurosci 19: 5085-5095, 1999. Webber RM, Stanley GB. Transient and steady-state dynamics of cortical adaptation. J Neurophysiol 95: 2923-2932, 2006. Welker WI. Analysis of the sniffing of the albino rat. Behaviour 22: 223-244, 1964. Report 3824 M. J. HIGLEY AND D. CONTRERAS
doi:10.1152/jn.00098.2007 pmid:17376853 fatcat:yejrnawfn5hrjknbvlrte3jkpy