Anatomical aspects of information processing in primate basal ganglia

doi:10.1016/0166-2236(93)90135-9

Trends in Neurosciences

Volume 16, Issue 3, March 1993, Pages 111-116

https://doi.org/10.1016/0166-2236(93)90135-9 Get rights and content

Abstract

Recent studies with double-anterograde tract-tracing methods have shed new light on the organization of the basal ganglia circuitry in primates. This paper briefly reviews some of these findings and provides a personal interpretation of their possible functional significance. Emphasis is placed on the fact that the striatum and the subthalamic nucleus have multiple representations in the two major output structures of the basal ganglia, namely the internal segment of the globus pallidus and the substantia nigra pars reticulata. It is hypothesized that this multiple representation serves as a means of amplifying and diversifying the striatal and subthalamic influences upon thalamocortical neurons that is mediated through the globus pallidus and the substantia nigra. Furthermore, evidence for the highly ordered organization of the striatopallidal and subthalamopallidal projections, which converge onto single pallidal neurons according to different but highly specific patterns, is taken as an indication that the subthalamic nucleus uniformly excites a vast collection of pallidal neurons, whereas the striatum exerts a more specific inhibitory control upon selected subsets of subthalamically driven pallidal neurons.

References (37)

A. Parent
Trends Neurosci.
(1990)
Y. Smith et al.
Brain Res.
(1988)
H. Nakanishi et al.
Brain Res.
(1991)
A.M. Graybiel
Trends Neurosci.
(1990)
G.E. Alexander et al.
Trends Neurosci.
(1990)
L-N. Hazrati et al.
Brain Res.
(1992)
L-N. Hazrati et al.
Brain Res.
(1992)
L-N. Hazrati et al.
Brain Res.
(1992)
C.J. Wilson et al.
Brain Res.
(1982)
A. Parent et al.
Brain Res.
(1984)

A. Parent et al.

Neurosci. Lett.

(1989)

S.N. Haber et al.

Neuroscience

(1981)

H. Kita

Brain Res.

(1992)

L-N. Hazrati et al.

Brain Res.

(1990)

L.D. Selemon et al.

J. Neurosci.

(1985)

A. Parent

Comparative Neurobiology of the Basal Ganglia

(1986)

S.T. Kitai et al.

C.E. Ribak et al.

J. Comp. Neurol.

(1979)

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The hyperdirect pathway. The hyperdirect pathway is a purported monosynaptic input pathway to the basal ganglia that bypasses typical input nuclei of the indirect pathway (outlined above) to directly innervate the STN (Parent and Hazrati, 1993; Nambu et al., 2002; Brunenberg et al., 2012; Chen et al., 2020). This is followed by glutamatergic innervation of SNr by the STN.
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The stop-signal task (SST) is used to study action-stopping in the laboratory. In SSTs, the P3 event-related potential following stop-signals is considered to be a neural index of motor inhibition. However, a similar P3 deflection is often observed following infrequent events in non-inhibition tasks. Moreover, within SSTs, stop-signals are indeed infrequent events, presenting a systematic confound that hampers the interpretation of the stop-signal P3 (and other candidate neural indices of motor inhibition). Therefore, we performed two studies to test whether the stop-signal P3 is uniquely related to motor inhibition or reflects infrequency detection. In Study 1, participants completed the SST and a visually identical change-detection task requiring the detection of a task-relevant, frequent signal (but not motor inhibition). We observed a P3 associated with motor inhibition in the SST, but no such positivity in the change-detection task. In Study 2, we modified the change-detection task. Some task-relevant events were now infrequent, matching the frequency of stop-signals in the SST. These events indeed evoked a P3, though of smaller amplitude than the P3 in the SST. Independent component analysis suggested that stop-signal P3 and infrequency-P3 ERPs were non-independent and shared a common neural generator. Further analyses suggested that this common neural process likely reflects motor inhibition in both tasks: infrequent events in the change-detection task lead to a non-instructed, incidental slowing of motor responding, the degree of which was strongly correlated with P3 amplitude. These results have wide-reaching implications for the interpretation of neural signals in both stop-signal and infrequency/oddball-tasks.
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Citation Excerpt :
The fact that a lesion of such a small nucleus can have such a dramatic effect points toward broad suppressive capabilities of the STN. Second, the STN-to-GPi projection appears to be relatively divergent; tracing studies from STN-GPi versus striatum-GPi showed that STN neurons have a broader innervation (Parent and Hazrati, 1993). Third, based on the finding of widespread STN collaterals and computational modeling, it has been theorized that activation of any one part of the STN ramifies throughout the nucleus, leading to a “massive suppressive pulse” on basal ganglia output (Gillies and Willshaw, 1998).
Unexpected events are part of everyday experience. They come in several varieties—action errors, unexpected action outcomes, and unexpected perceptual events—and they lead to motor slowing and cognitive distraction. While different varieties of unexpected events have been studied largely independently, and many different mechanisms are thought to explain their effects on action and cognition, we suggest a unifying theory. We propose that unexpected events recruit a fronto-basal-ganglia network for stopping. This network includes specific prefrontal cortical nodes and is posited to project to the subthalamic nucleus, with a putative global suppressive effect on basal-ganglia output. We argue that unexpected events interrupt action and impact cognition, partly at least, by recruiting this global suppressive network. This provides a common mechanistic basis for different types of unexpected events; links the literatures on motor inhibition, performance monitoring, attention, and working memory; and is relevant for understanding clinical symptoms of distractibility and mental inflexibility.

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Trends in Neurosciences

ReviewAnatomical aspects of information processing in primate basal ganglia

Abstract

Trends Neurosci.

Brain Res.

Brain Res.

Trends Neurosci.

Trends Neurosci.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Neuroscience

Brain Res.

Brain Res.

J. Neurosci.

Comparative Neurobiology of the Basal Ganglia

J. Comp. Neurol.

Review
Anatomical aspects of information processing in primate basal ganglia