The Role of the Monkey Dorsal Pontine Nuclei in Goal-Directed Eye and Hand Movements

Abstract

Prevailing concepts on the control of goal-directed hand movements (HM) have focused on a network of cortical areas whose early parieto-occipital stages are thought to extract and integrate information on target and hand location, involving subsequent stages in frontal cortex forming and executing movement plans. The substantial experimental results supporting this "cortical network" concept for hand movements notwithstanding, the concept clearly needs refinement to account for the surprisingly mild HM disturbances resulting from disconnecting the parieto-occipital from the frontal stages of the network. Clinical observations have suggested the cerebropontocerebellar projection as an alternative pathway for the sensory guidance of HM. As a first step in assessing its role, we explored the pontine nuclei (PN) of rhesus monkeys, trained to make goal-directed hand and eye movements guided by spatial memory. We were indeed able to delineate a distinct cluster of neurons in the rostrodorsal PN, activated by the preparation and the execution of hand reaches, close to but distinct from the region in which saccade-related neurons may be observed. The movement-related activity of HM-related neurons starts earlier than that of saccade-related neurons and both neuron types are usually effector specific, i.e., they respond only to the movement of the preferred effector. This is also the case when motor synergies involving both effectors are executed. Our findings support the notion of a distinct precerebellar, pontine visuomotor channel for hand reaches that is anatomically and functionally largely separated from the one serving eye movements.

Dendritic Nonlinearities Reduce Network Size Requirements and Mediate ON and OFF States of Persistent Activity in a PFC Microcircuit Model

“…This ability to predict ON and OFF states is in agreement with previous modeling (albeit with a different feature) work [23] and conforms with experimental work [51] showing that single neurons can encode state transitions, and PFC neurons in particular, can categorize signals in vivo at the onset of stimulus presentation [52]. This information is readily available to downstream regions [53], [54], presumably contributing to the preparation of a specific movement.…”

Cerebellum-Dependent Motor Learning

“…Both the DPN and the NRTP contribute to saccades as well as to SPEMs, deploying oculomotor neurons that vary regarding the degree of sensitivity for either type of visually guided eye movements (Crandall and Keller, 1985;Dicke et al, 2004;Suzuki et al, 1999;Thier and Mock, 2006;Thier et al, 1988;Tziridis et al, 2009). In view of this input, it is not surprising that also the OMV sports saccadeas well as pursuit-related PCs-the only output neuron of cerebellar cortex.…”

Diverse Precerebellar Neurons Share Similar Intrinsic Excitability

“…Precerebellar mossy fiber neurons are remarkably diverse with respect to both the stimuli they respond to and their firing responses in vivo (Eccles et al, 1971; Lisberger and Fuchs, 1978; Noda, 1986; van Kan et al, 1993; Zhang et al, 1995; Cheron et al, 1996; Escudero et al, 1996; Garwicz et al, 1998; Mackie et al, 1999; Rancz et al, 2007; Bengtsson and Jorntell, 2009; Tziridis et al, 2009; Tziridis et al, 2011). For example, neurons in the external cuneate nucleus fire transient, high frequency bursts in response to direct sensory (cutaneous) stimulation (Bengtsson and Jorntell, 2009), while those in the prepositus hypoglossi exhibit graded modulations in firing rate that are proportional to eye position (Escudero et al, 1996).…”

“…For example, neurons in the external cuneate nucleus fire transient, high frequency bursts in response to direct sensory (cutaneous) stimulation (Bengtsson and Jorntell, 2009), while those in the prepositus hypoglossi exhibit graded modulations in firing rate that are proportional to eye position (Escudero et al, 1996). Neurons in pontine nuclei are driven by complex cortical signals and exhibit a wide range of firing responses even during simple sensory-motor tasks (Tziridis et al, 2009, 2011). …”