Abstract
Dysfunction of the basal ganglia produces severe deficits in the timing, initiation, and vigor of movement. These diverse impairments suggest a control system gone awry. In engineered systems, feedback is critical for control. By contrast, models of the basal ganglia highlight feedforward circuitry and ignore intrinsic feedback circuits. In this study, we show that feedback via axon collaterals of substantia nigra projection neurons control the gain of the basal ganglia output. Through a combination of physiology, optogenetics, anatomy, and circuit mapping, we elaborate a general circuit mechanism for gain control in a microcircuit lacking interneurons. Our data suggest that diverse tonic firing rates, weak unitary connections and a spatially diffuse collateral circuit with distinct topography and kinetics from feedforward input is sufficient to implement divisive feedback inhibition. The importance of feedback for engineered systems implies that the intranigral microcircuit, despite its absence from canonical models, could be essential to basal ganglia function. DOI: http://dx.doi.org/10.7554/eLife.02397.001.
Highlights
The basal ganglia are a collection of interconnected subcortical regions of the vertebrate brain (DeLong, 2000)
Feedback projections of SNr neurons provides a source of negative feedback, we would expect that the level of activation of the population immediately prior to a stimulus should be inversely correlated with the modulation of the response of an individual neuron to that stimulus
We computed the normalized response to a salient stimulus as a function of the normalized activity of the simultaneously recorded population of neurons for 32 recording sessions in which at least eight neurons were recorded simultaneously for each trial in the recording session (Figure 1A–B). This yielded a data set of 28,277 comparisons from which we estimated the correlation between the activation of the population at baseline to the activation of each individual neuron in response to the conditioned stimulus (CS)
Summary
The basal ganglia are a collection of interconnected subcortical regions of the vertebrate brain (DeLong, 2000). Pathological disruptions of basal ganglia signaling produce profound deficits in the timing (Buhusi and Meck, 2005), vigor (Turner and Desmurget, 2010), and initiation (Mink, 1996) of voluntary movements. While it is clear that the basal ganglia are critical for voluntary movement, the specific mechanisms by which movement is controlled by basal ganglia activity remain unclear (Turner and Desmurget, 2010). The basal ganglia circuit can be described as an extended loop that begins with projections from deep layer cortical neurons and returns to the cortex via projections from the basal ganglia to the ventral thalamus (Haber, 2003). The basal ganglia circuit contains intrinsic feedback projections (Gerfen, 2004). Feedback is critical for stable performance (Astrom and Murray, 2008)
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