Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys

Abstract

Nuclei within the basal ganglia (BG), in particular the substantia nigra pars reticulata (SNr), subthalamic nucleus (STN) and caudate nucleus, are known to be involved in the generation of rapid or saccadic eye movements. Neurons in the SNr are active tonically and generally show a pause, but also increase, in discharge rate, for the appearance of visual stimuli and the generation of saccades. Recent experimental results in oculomotor regions of the brainstem reveal overlap in the neuronal pathways used for saccades and smooth pursuit, or slow tracking, eye movements. Whether the overlap of processing for saccades and pursuit extends to the oculomotor BG is unknown. In the present report, we were interested in whether the overlap between the pursuit and saccadic systems extends into the oculomotor BG. Using single-neuron recording and electrical stimulation techniques, we tested whether neurons within the saccade portion of the BG, the SNr, could be involved in smooth pursuit eye movements. Monkeys were required to follow visual targets with either a smooth eye movement or a saccade while we recorded from SNr neurons. We report here on SNr neuronal activity that was modulated during the performance of visually guided saccades and also during the initiation and the maintenance of smooth pursuit eye movements. Importantly, the modulation of neuronal activity during pursuit was present even when catch-up saccades were absent. The majority of SNr neurons was active tonically and their discharge ceased during pursuit, although some neurons also increased their discharge rate during smooth pursuit, similar to the behaviour reported for saccades. We also found that electrical stimulation of the SNr during the initiation of pursuit suppressed ipsiversive and, in some cases, enhanced contraversive pursuit. Our combined recording and stimulation results are consistent with the hypothesis that the overlap between the pursuit and saccadic systems extends, at least somewhat, into the BG and that the signal conveyed by the SNr can be used by the pursuit system. Like the signal for saccades, the SNr may provide a permissive disinhibition for pursuit eye movements. We hypothesize that alterations in this signal in BG diseased states such as Parkinson's may explain in part the deficits observed in smooth pursuit eye movements of these patients.

Neural effects of methylphenidate and nicotine during smooth pursuit eye movements

“…Cholinergic stimulation of superior colliculus leads to improved initiation of eye movements (Aizawa et al, 1999), whereas electrical stimulation of substantia nigra operates bidirectionally and either suppresses or enhances pursuit movement (Basso et al, 2005). While these structures are potential action sites of the present pharmacological challenge, on the basis of our findings their involvement in the observed drug effect remains suggestive.…”

Neuronal activity in the primate globus pallidus during smooth pursuit eye movements

“…The firing rate of many of these neurons was modulated during pursuit in opposite directions, and neuronal activity often persisted even after target motion, suggesting that the neuronal activity was strictly related neither to the direction nor to the speed of pursuit. Similar to neurons in the SNr [12] and in the thalamus [15], most pursuit-related neurons in the GP also modulated firing during saccades to a stationary target. Importantly, however, the firing modulation during pursuit was present even in the absence of catch up saccades.…”

“…Because both neurons exhibited firing modulation for trials without early saccade (raster lines with left bracket), the activity during pursuit was not solely due to the occurrence of catch up saccades. Although the neuronal modulation during pursuit was observed even when catch up saccades were absent, most pursuit-related neurons in the GP also responded to saccades to a stationary target, like neurons in the SNr [12] and in the thalamus [15]. When neuronal activity during saccades of 16° was examined, 83% neurons (n = 33/38 increase-type neurons; n = 32/40 decrease-type neurons) exhibited clear firing modulation.…”

“…Despite these observations, the firing of single neurons in the basal ganglia during pursuit has not been examined, with the exception of one recent study that explored signals in the substantia nigra pars reticulata (SNr) [12]. As a step toward understanding the roles of the basal ganglia in smooth pursuit, we examined neuronal activity in the globus pallidus (GP) in monkeys.…”

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

“…Several lines of evidence suggested that the SNr plays critical roles in the control of saccadic eye movements (Handel and Glimcher, 1999;Basso and Wurtz, 2002;Bayer et al, 2004;Basso et al, 2005;Basso and Liu, 2007). One of the interesting observations reported by Basso and Liu (2007) is that electrical stimulation of the SNr both reduced and prolonged saccade latency.…”