Substantia Nigra Stimulation Influences Monkey Superior Colliculus Neuronal Activity Bilaterally

Abstract

Liu P, Basso MA. Substantia nigra stimulation influences monkey superior colliculus neuronal activity bilaterally. J Neurophysiol 100: 1098 -1112, 2008. First published June 25, 2008 doi:10.1152/jn.01043.2007. The inhibitory drive arising from the basal ganglia is thought to prevent the occurrence of orienting movements of the eyes, head, and body in monkeys and other mammals. The direct projection from the substantia nigra pars reticulata (SNr) to the superior colliculus (SC) mediates the inhibition. Since the original experiments in the SNr of monkeys the buildup or prelude neuron has been a focus of SC research. However, whether the SNr influences buildup neurons in SC is unknown. Furthermore, a contralateral SNr-SC pathway is evident in many species but remains unexplored in the alert monkey. Here we introduced electrical stimulation of one or both SNr nuclei while recording from SC buildup neurons. Stimulation of the SNr reduced the discharge rate of SC buildup neurons bilaterally. This result is consistent with activation of an inhibitory drive from SNr to SC. The time course of the influence of ipsilateral SNr on the activity of most SC neurons was longer (ϳ73 ms) than the influence of the contralateral SNr (ϳ34 ms). We also found that the variability of saccade onset time and saccade direction was altered with electrical stimulation of the SNr. Taken together our results show that electrical stimulation activates the inhibitory output of the SNr that in turn, reduces the activity of SC buildup neurons in both hemispheres. However, rather than acting as a gate for saccade initiation, the results suggest that the influence of SNr inhibition on visually guided saccades is more subtle, shaping the balance of excitation and inhibition across the SC.

Alterations to multisensory and unisensory integration by stimulus competition

“…Likewise, recent studies have demonstrated that the substantia nigra pars reticulata (SNr), in addition to its well-known inhibitory projection to the ipsilateral SC (Chevalier et al 1984;Hikosaka and Wurtz 1983;Karabelas and Moschovakis 1985;May and Hall 1984), provides a crossed inhibitory input to the opposite SC Liu and Basso 2008). Critically, these SNr projections perform complementary functions, simultaneously facilitating contralateral stimulus/movement representations (via disinhibition) while suppressing those to the ipsilateral side.…”

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

“…A second set of studies suggesting a broader role for SNr input to the SC examined the anatomy and physiology of this input. First, while the disinhibition model is based on ipsilaterally projecting (i.e., "uncrossed") nigrotectal neurons, some ("crossed") nigrotectal neurons project contralaterally (Beckstead et al 1981;Chevalier et al 1981;Deniau et al 1977;Gerfen et al 1982;Jayaraman et al 1977;Liu and Basso 2008) and a small number project to both SCs (Cebrián et al 2005). Given that crossed nigrotectal projections are also inhibitory, they would appear to promote movements ipsiversive to the phasically inactivated SNr, inconsistent with the disinhibition model.…”

“…Given that crossed nigrotectal projections are also inhibitory, they would appear to promote movements ipsiversive to the phasically inactivated SNr, inconsistent with the disinhibition model. Second, in addition to the influence of SNr activity on bursting SC neurons that initiate movements (Hikosaka and Wurtz 1983), SNr input modulates the activity of buildup SC neurons (Liu and Basso 2008) thought to subserve the selection of targets for movement (but see Corneil et al 2007). Finally, uncrossed nigrotectal neurons project to GABAergic SC neurons-which, as discussed above, may mediate the inhibition between SC circuits representing competing movements-as often as they project to glutamatergic SC neurons (Kaneda et al 2008), further suggesting a broader role for the SNr than simple disinhibition.…”

Similarity of superior colliculus involvement in microsaccade and saccade generation

“…Through local excitation, this differential activation could get amplified and gradually lead to elevated firing rates until a movement is triggered. Alternately, modulation of inhibitory input (e.g., from substantia nigra; Hikosaka and Wurtz 1985;Isa and Hall 2009;Liu and Basso 2008) or excitatory input (e.g., from the prefrontal cortex; Sommer and Wurtz 2000;Wurtz et al 2001) could shape SC population activity and contribute to microsaccade-related buildup. These mechanisms are sources of saccade-related buildup of activity elsewhere in the SC, highlighting the similarity between microsaccades and saccades at the mechanistic level.…”