Opposing Excitatory and Inhibitory Influences from the Cerebellum and Basal Ganglia Converge on the Superior Colliculus: an Electrophysiological Investigation in the Rat

Abstract

We recently showed (Westby et al., Eur. J. Neurosci., 5, 1378-1388, 1993) that the cerebellar interpositus nucleus is a source of excitatory drive for a population of spontaneously active neurons in the lateral intermediate layers of the contralateral superior colliculus. Anatomical and physiological studies have shown that this region of the colliculus contains cells of origin of the crossed descending tectoreticulospinal tract and receives GABAergic input from the ipsilateral basal ganglia. In the present study we tested the hypothesis that the same neurons receiving excitatory drive from the cerebellum also receive tonic inhibitory input from the substantia nigra pars reticulata. From a sample of 73 spontaneously active collicular cells we found that in 53% the firing rate was suppressed by GABA microinjection into the contralateral deep cerebellar nuclei; a further 15% showed a frequency increase. Of the collicular cells identified as receiving excitatory cerebellar input, 85% were found to be disinhibited by nigral GABA microinjection. The remainder were all inhibited by nigral GABA. These data show that the main excitatory influence from the cerebellum and the main inhibitory influence from the substantia nigra converge on at least one population of spontaneously active cells in the lateral intermediate layers of the superior colliculus. This finding is discussed in relation to the possible function of these spontaneous cells in movement control and nociception.

An integrative role for the superior colliculus in selecting targets for movements

“…For example, cerebellar nuclei provide excitatory input to the same SC neurons that receive inhibition from the SNr (Westby et al 1994), and inhibition of the cerebellar caudal fastigial nucleus alters gaze direction during fixation (Guerrasio et al 2010) and disrupts gaze fixation in the presence of a competing target (Fukushima et al 2011). These findings demonstrate a cerebellar contribution to SC-mediated fixation and its release (Goffart et al 2012;Quinet and Goffart 2015).…”

Thalamic interactions of cerebellum and basal ganglia

“…Such a network comprises structures of the brainstem (reticular formation, superior colliculus, and red nucleus), thalamus (CM/Pf, MD), basal ganglia, and cortex (frontal eye fields). Nigral and cerebellar projections have been shown to converge on neurons of the superior colliculus in the rat (Westby et al 1994). Similarly, these two structures seem to interact in the reticular formation (ShammahLagnado et al 1983(ShammahLagnado et al , 1987(ShammahLagnado et al , 1992Schneider et al 1985) and the nucleus of Darkschewitsch, which has been associated with the red nucleus based on its similar connectivity patterns (Onodera and Hicks 2009, 1998.…”

“…Similar projections of the basal ganglia to the cerebellum have been shown to originate in the subthalamic nucleus, being relayed to the cerebellar cortex via pontine nuclei and/or tegmental pontine reticular nucleus . Further evidence of subcortical interaction exists in the brainstem [e.g., superior colliculus in Westby et al (1994)] and in the thalamus (Chevalier and Deniau 1982;Nambu et al 1988;Sakai and Patton 1993;Sakai et al 1996). However, discrepancies exist concerning the amount of these convergences.…”

Invited Review Anatomical loops and their electrical dynamics in relation to whisking by rat

“…(cerebellum ® superior colliculus) The deep cerebellar nuclei send a projection to the colliculus (Lee et al, 1989;Westby et al, 1993Westby et al, , 1994, which forms a ª colliculus ® cerebellum ® colliculusº loop.…”

“…For completeness, we note that the basal ganglia also form a closed loop with the superior colliculus. The colliculus sends projections to the basal ganglia (Tokuno et al, 1994), and the basal ganglia send inhibitory connections to the colliculus (Faull and Mehler, 1978;Gerfen et al, 1982;Westby et al, 1993Westby et al, , 1994Niemi-Junkola and Westby, 1998); the role of the basal ganglia in whisking is presently unclear. 4.…”