Quantitative Analysis of Substantia Nigra Pars Reticulata Activity During a Visually Guided Saccade Task

Abstract

Several lines of evidence suggest that the pars reticulata subdivision of the substantia nigra (SNr) plays a role in the generation of saccadic eye movements. However, the responses of SNr neurons during saccades have not been examined with the same level of quantitative detail as the responses of neurons in other key saccadic areas. For this report, we examined the firing rates of 72 SNr neurons while awake-behaving primates correctly performed an average of 136 trials of a visually guided delayed saccade task. On each trial, the location of the visual target was chosen randomly from a grid spanning 40 degrees of horizontal and vertical visual angle. We measured the firing rates of each neuron during five intervals on every trial: a baseline interval, a fixation interval, a visual interval, a movement interval, and a reward interval. We found four distinct classes of SNr neurons. Two classes of neurons had firing rates that decreased during delayed saccade trials. The firing rates of discrete pausers decreased after the onset of a contralateral target and/or before the onset of a saccade that would align gaze with that target. The firing rates of universal pausers decreased after fixation on all trials and remained below baseline until the delivery of reinforcement. We also found two classes of SNr neurons with firing rates that increased during delayed saccade trials. The firing rates of bursters increased after the onset of a contralateral target and/or before the onset of a saccade aligning gaze with that target. The firing rates of pause-bursters increased after the onset of a contralateral target but decreased after the illumination of an ipsilateral target. Our quantification of the response profiles of SNr neurons yielded three novel findings. First, we found that some SNr neurons generate saccade-related increases in activity. Second, we found that, for nearly all SNr neurons, the relationship between firing rate and horizontal and vertical saccade amplitude could be well described by a planar surface within the range of movements we sampled. Finally we found that for most SNr neurons, saccade-related modulations in activity were highly variable on a trial-by-trial basis.

Attentional Modulation of Thalamic Reticular Neurons

“…This high background rate is similar to that in another area where the output is inhibitory, the substantia nigra pars reticulata (Hikosaka and Wurtz, 1983;Hikosaka et al, 2000). Unlike the substantia nigra where the response to a visual stimulus is usually a transient pause in activity, with only some neurons showing a rise in activity (Handel and Glimcher, 1999), the response in TRN is consistently a transient increase of activity. Therefore, although the substantia nigra and the TRN both provide inhibitory outputs, the substantia nigra removes inhibition in response to visual stimuli, whereas the TRN produces a transient increase in inhibition.…”

Subcortical processes of motor response inhibition during a stop signal task

“…Notably, although the connections within the cortico-striato-thalamic "loops" are well defined chemically (excitatory or inhibitory), none of them have individually been assigned a specific role in motor response inhibition. For instance, despite the focus of earlier unit recording studies on saccade-related tonic-pause neurons, more recent work have documented saccade-related "burst" neuronal responses, in the pars reticulata of the substantia nigra, an output nucleus of the basal ganglia (Bayer et al, 2004;Handel and Glimcher, 1999;Handel and Glimcher, 2000;Hikosaka and Wurtz, 1983a;Hikosaka and Wurtz, 1983b;Sato and Hikosata, 2002).…”

Balance of Increases and Decreases in Firing Rate of the Spontaneous Activity of Basal Ganglia High-Frequency Discharge Neurons

“…In contrast to this anatomical dominance of inhibitory input, physiological studies consistently report that most (60 -80%) of the pallidal neurons increase their firing rate in response to behavioral events (Brotchie et al 1991;Georgopoulos et al 1983;Jaeger et al 1995;Mink and Thach 1991;Mitchell et al 1987;Turner and Anderson 1997). Neurons of the SNr belong to the same morphological type as pallidal neurons (Fox et al 1974;Yelnik et al 1987), receive similar anatomical inputs Rinvik and Grofova 1970), and as in the pallidum their behavioral-related activity is not dominated by a decrease in firing rate (Handel and Glimcher 1999;Nevet et al 2007;Sato and Hikosaka 2002;Schultz 1986). Additionally, the soma of neurons in the GPi and the SNr (the output structures) as well as the GPe itself is innervated by GPe GABAergic synapses (Kincaid et al 1991;Sadek et al 2007;Smith and Bolam 1989).…”