Responses of Cerebellar Interpositus Neurons to Predictable Perturbations Applied to an Object Held in a Precision Grip

Abstract

Two monkeys were trained to lift and hold an instrumented object at a fixed height for 2.5 s using a precision grip. The device was equipped with load cells to measure both the grip and lifting or load forces. On selected blocks of 20-30 trials, a downward force-pulse perturbation was applied to the object after 1.5 s of stationary holding. The animals were required to resist the perturbation to obtain a fruit juice reward. The perturbations invariably elicited a reflex-like, time-locked increase in grip force at latencies between 50 and 100 ms. In this study, we searched for single cells in the interpositus and dentate nuclei with activity related to grasping and lifting, and we tested 127/150 task-related cells for their responses to the perturbation. Of the 127 cells, reflex-like increases or decreases in discharge frequency occurred in 75 cells (59%) at a mean latency of 36 ms. Preparatory increases in grip force preceding the perturbation appeared gradually and increased in strength with repetition in 39/127 (31%) cells. These preparatory increases did not immediately disappear when the perturbations were withdrawn but decreased progressively over repeated trials. Although a few cells showed anticipatory activity without a reflex-like response (15/127 or 12%), the majority of these cells (24/39) displayed both anticipatory and reflex-like responses. From an examination of the histological sections, cells with both anticipatory and reflex-like responses appeared to be confined to the dorsal anterior interpositus, adjacent to, but not within, the dentate nucleus. These results confirm and extend the suggestion by Dugas and Smith that the cerebellum plays a major role in organizing anticipatory responses to predictable perturbations in a manner that medial and lateral premotor areas of the cerebral cortex do not.

Lighter or Heavier Than Predicted: Neural Correlates of Corrective Mechanisms during Erroneously Programmed Lifts

“…Likewise, by comparing the brain activity in trials performed with a light weight, but programmed for a heavier weight, with trials that were adequately programmed for a light weight, we could elucidate the neural substrates responsible for the abrupt termination of the fingertip force that occurs after the premature lift off (Johansson and Westling, 1988). We hypothesized that the primary sensorimotor cortex and the cerebellum would be involved in these corrective mechanisms because they receive strong somatosen-sory input from the fingertips and control hand muscle activity (Picard and Smith, 1992;Maier et al, 1993;Dettmers et al, 1995;Lemon et al, 1998;Monzee and Smith, 2004) Brain areas that were activated during the unpredictable weight changes, regardless of whether the weight is heavier or lighter, would likely represent neural circuits involved in the mismatch detection between the predicted and actual sensory information and the subsequent updating of the sensorimotor memories (Johansson, 1998;Wolpert and Ghahramani, 2000). Based on previous studies, we hypothesized that the cerebellum (Doya, 1999;Kawato, 1999;Blakemore et al, 2001), and frontal and parietal areas associated with object manipulation (Schmitz et al, 2005), would show such increases in synaptic activity.…”

Cerebellar ataxia impairs modulation of arm stiffness during postural maintenance

“…Discharge frequency of task-related dentate and interposed nuclei increased with cocontraction of the forearm muscles (Wetts et al 1985), whereas Purkinje cells decreased their firing (Frysinger et al 1984). Monzee and Smith (2004) also trained monkeys to hold an object at a fixed position while resisting force perturbations. Activity in approximately one-third of the recorded interposed and dentate nuclei gradually increased as the monkeys learned to produce preparatory increases in grip force and wrist stiffness prior to the predictable perturbations.…”

Anticipatory Vibrotactile Cueing Facilitates Grip Force Adjustment during Perturbative Loading

“…Cutaneous inputs usually reach the somatosensory cortex in a few tens of milliseconds [46], whereas the experience of perception arises 23-550 ms after stimulation [47], [48]. In a study of grip adjustment in monkeys, reflex-like changes in cerebellar cortical neurons appeared with an average latency of 36 ms after the onset of a perturbative load to the gripped object [49]. These reports suggest that motor preparation does not necessarily start after the cognition of sensory stimuli, and that the stimulus may affect motor responses before it is even consciously recognized [48].…”