Functional dynamics of primate cortico-striatal networks during volitional movements

Abstract

The motor cortex and dorsal striatum (caudate nucleus and putamen) are key regions in motor processing but the interface between the cortex and striatum is not well understood. While dorsal striatum integrates information from multiple brain regions to shape motor learning and habit formation, the disruption of cortico-striatal circuits compromises the functionality of these circuits resulting in a multitude of neurologic disorders, including Parkinson's disease. To better understand the modulation of the cortico-striatal circuits we recorded simultaneously single neuron activity from four brain regions, primary motor, and sensory cortices, together with the rostral and caudal segments of the putamen in rhesus monkeys performing a visual motor task. Results show that spatial and temporal-task related firing relationships between these cortico-striatal circuit regions were modified by the independent administration of the two drugs (cocaine and baclofen). Spatial tuning and correlated firing of neurons from motor cortex and putamen were severely disrupted by cocaine and baclofen on correct trials, while the two drugs have dramatically decreased the functional connectivity of the motor cortical-striatal network. These findings provide insight into the modulation of cortical-striatal firing related to movement with implications for therapeutic approaches to Parkinson's disease and related disorders.

Processing of sub- and supra-second intervals in the primate brain results from the calibration of neuronal oscillators via sensory, motor, and feedback processes

“…The correlated firing behavior is consistent with the accurate transmission of information (Santos et al, 2014), which is necessary for a feedback mechanism. Another study showed coherence during the simultaneous recordings of the electrocorticogram and local field potential in the basal ganglia (Magill et al, 2004).…”

“…A study that simultaneously recorded single neuron activities from the primary motor and sensory cortex together with the putamen during a visual motor task, found spatial and temporal task-related firing of neurons across these regions (Santos et al, 2014). The correlated firing behavior is consistent with the accurate transmission of information (Santos et al, 2014), which is necessary for a feedback mechanism.…”

Disruption of columnar and laminar cognitive processing in primate prefrontal cortex following cocaine exposure

“…These neural recordings demonstrate that prefrontal neurons differentially encode and process information within and between cortical cell layers via cortical columns which are disrupted in a differential manner by cocaine administration. Such cocaine driven disruption may be explained by a selective reduction of the excitatory synaptic inputs to pyramidal neurons by a selective D1 receptor (Bourne, 2001 ; Urban et al, 2002 ; Rebec and Sun, 2005 ; Stuber et al, 2005 ; Volkow et al, 2005 ; Tomasi et al, 2010 ; Porrino et al, 2013 ; Santos et al, 2014 ) with inverted-U dose curve/actions (Vijayraghavan et al, 2007 ). This view is in agreement to recent studies showing that prefrontal dopamine D1 receptors control visual signals during attention and modulation of memory fields in working memory (Williams and Goldman-Rakic, 1995 ; Vijayraghavan et al, 2007 ; Noudoost and Moore, 2011 ).…”

Advancing brain-machine interfaces: moving beyond linear state space models

“…Yet the size of synchrony effects also can change rapidly when novel motor behaviors are being performed (Davidson et al, 2007 ), suggesting that different common inputs to the population of neurons with last-order inputs to a given motoneuron pool become active in different contexts, again indicating different neural trajectories for different contexts. These rapid changes depending on context may involve processing in cortical minicolumns and corticostriatal circuits, where the level of functional connectivity (as measured by cross-correlations between simultaneously recorded spikes in layer 2/3 and layer 5 of a minicolumn, for example) has been found to vary with the type and difficulty of the task being performed (Opris et al, 2012 , 2013 ; Santos et al, 2014 ). For optimal performance, BMIs will need to take into account such context-dependent changes in neuron activity and the changes in neural trajectories they represent.…”