Motor Information in Dorsolateral Striatum Neurons

Fig. 1

A juxtacellularly recorded striatum neuron. (a) Fluorescent visualization for Neurobiotin-loaded neuron. (b) In situ hybridization for dopamine D1 receptor mRNA. (c) Its re-stained morphology

Next, we examined whether the functional activity of motor cortex neurons was affected by the reward alternation, because the striatal reward information may be conveyed from the motor cortex rather than the substantia nigra. Using the multi-neuronal recording, we obtained a total of 216 neurons (164 regular-spiking (RS) and 52 fast-spiking (FS) neurons) in the FL area of the motor cortex during the task performance (N = 24 rats) [3]. We found 46 Hold-type and 106 Movement-type neurons in the motor cortex. Consistent with our previous study [4], many of the FS neurons displayed the Movement-type activity (n = 37) rather than the Hold-type activity (n = 1). Importantly, most of the motor cortex neurons were not clearly modulated by the reward alternation. The cortico-striatal pyramidal cells are located in the layers 5A and 5B of the rat motor cortex. We found no largely biased distribution in the reward modulation of Movement-type activity in the superficial (putatively layer 2/3), middle (layer 5), and deep (layer 6) layer subpopulations. It suggests that most of motor cortex neurons appeared be specialized to process motor information with no reward information, unlike the striatal neurons.

4 Discussion

As described above, we showed how motor information and reward information are represented by individual neurons in the dorsolateral striatum and the motor cortex of the skeletomotor loop in the rat. According to the classical basal ganglia model, the excitation of striatal neurons for the direct and indirect pathways, respectively, enhances and depresses the activity of motor cortical neurons antagonistically [1]. Recent studies using gene modification techniques certainly support this model [8, 9]. Therefore, one may expect that the direct pathway neurons increase the spike activity during voluntary movements, whereas the indirect pathway neurons do so during no movements. However, no large difference was found between D1-positive and -negative neurons in the dorsolateral striatum. Interestingly, Cui et al. (2013) reported that these two pathways are concurrently and similarly activated during voluntary movements [10]. Our results at a single-cell resolution level favor their observations.

Thus, the antagonistic pathway system may be accomplished by a more complex involvement of the two groups of striatal neurons. For example, for Hold-type activity, D1-positive (direct pathway) neurons may prepare for an intended movement or just maintain overall muscle tone, while D1-negative (indirect pathway) neurons may suppress temporally incorrect expression of the movement. For Movement-type activity, D1-negative neurons may suppress concurrent expression of antagonistic muscular movements, while D1-positive neurons execute the intended movement. Taken together, this simple movement may actually be composed of several spatiotemporal motor components, and individual striatal neurons for both pathways may antagonistically code subprograms for the motor components to complete the whole movement coordinately.

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