The Influence of Somatosensory Cortex on Climbing Fiber Responses in the Lateral Hemispheres of the Rat Cerebellum after Peripheral Tactile Stimulation

Ian E. Brown, James M. Bower
2002 Journal of Neuroscience  
This report describes the temporal relationship between the latency of responses to peripheral stimulation in primary somatosensory (SI) cerebral cortex and the timing of climbing fiber inputs to the lateral hemispheres of the rat cerebellum. Examined in the tactilely responsive regions of crus IIa in the rat, the results show that SI influences the timing of both evoked and spontaneous climbing fiber activity in these cerebellar regions without affecting the rate or probability of complex
more » ... discharge. By reversibly blocking SI activity, we demonstrate that the absence of cortical input results in a lengthening of climbing fiber response latency to peripheral stimuli. Similarly, enhancing the cortical input by subthreshold electrical stimulation of SI results in a shortening of climbing fiber response latency. These results provide a new explanation for the tendency of the inferior olive to oscillate at 7-12 Hz and is consistent with the hypothesis that the inferior olive provides the cerebellum information about the timing of cortical computational cycles. Results are discussed in the context of previous and current hypotheses concerning the physiology and function of the inferior olive/climbing fiber system and are interpreted to provide additional evidence of a role for the cerebellum in the tactile somatosensory system. The climbing fiber system, with its sole origin in the inferior olive (IO) and its mono-axonal "climbing fiber" connection to Purkinje cells (Palay and Chan-Palay, 1974), plays a major role in many hypotheses of cerebellar function (Marr, 1969; Thach et al., 1992; Llinas and Welsh, 1993; Houk et al., 1996) . Given the predominance of the view that the cerebellum is primarily a motor control device (Bower, 1997a), most hypotheses for the function of the inferior olive and the climbing fiber system have focused on some link to motor performance. One prominent hypothesis, for example, proposes that climbing fiber discharges specifically signal motor performance errors to cerebellar Purkinje cells, which then change their output to improve motor performance (Kawato and Gomi, 1992) . Although this hypothesis does not clearly state how motor error is detected, it is assumed that the inferior olive is the relay for this information. Another proposal links the inferior olive directly to motor learning, suggesting that climbing fiber discharge triggers either the enhancement (Marr, 1969) or depression (Albus, 1971) of coincidently active parallel fibers. In this way it has been proposed that the climbing fiber system "instructs" Purkinje cells as to which of their 150,000 parallel fibers should influence output. A third more recent proposal suggests that climbing fiber firing is responsible for coordinating the timing of movement (Llinas and Welsh, 1993) . Whereas each of these hypotheses is somewhat different, they share in common the idea that the precise timing of climbing fiber discharge is critical to function and related directly to some aspect of movement. In the case of both the motor error and motor learning hypotheses, climbing fiber discharge is assumed to be generated by the detection of some specific motor-related event. In the case of the movement timing hypothesis, the intrinsic properties of the inferior olive itself are assumed to control the timing of climbing fiber activity. In each case, the timing of climbing fiber discharge is linked directly to some particular aspect of movement. Over the last several years, our laboratory has been investigating the possibility that cerebellar function may be more related to the internal needs of the nervous system than to the types of overt motor behavior proposed in classical hypotheses (Bower, 1997a,b). In particular, we have proposed that the cerebellum may be responsible for coordinating the acquisition of sensory data on which the rest of the nervous system depends. Although this hypothesis has derived primarily from our studies of mossy fiber tactile projections to cerebellar cortex (Bower and Woolston, 1983; Morissette and Bower, 1996) , we have recently begun to extend our investigations to include the climbing fiber system (Brown and Bower, 2001) . These studies have already demonstrated a strong similarity between the spatial pattern of mossy fiber and climbing fiber tactile projections to tactile regions of the lateral hemispheres in the rat (Brown and Bower, 2001) . In this paper we extend these initial studies to examine the all important question of the control of timing of climbing fiber activity. We have previously hypothesized (Bower, 1997a,b) that the 7-12 Hz oscillatory behavior of the inferior olive might be related directly to the fact that cerebral cortex oscillates at these particular frequencies. In this view, the inferior olive is proposed to be responsible for relaying information about the timing of cerebral cortical computational cycles rather than itself orchestrating anything having to do with movement performance.
doi:10.1523/jneurosci.22-15-06819.2002 pmid:12151562 fatcat:4j5gqw7nizcifejnrery6ditle