Relationships between sensory responsiveness and premovement activity of quickly adapting neurons in areas 3b and 1 of monkey primary somatosensory cortex

Abstract

When monkeys make wrist movements in response to vibration of their hands, primary somatosensory (SI) cortical neurons that adapt quickly to the vibratory stimulus often exhibit two temporally separate types of activity. Initially, these neurons respond to the stimulus. They then cease discharging, only to resume firing prior to the movement. This activation, cessation and reactivation occurs even though the sensory stimulus remains on until after the movement is begun. The first change in activity is most likely related to sensory input. The second, which has been called premovement activity, may have a sensory component as well as one related to the upcoming movement. We wanted to test the hypothesis that the premovement activity exhibited when vibration is present represents both a reactivation of a neuron's vibratory response and the premovement activity that normally occurs when vibration is absent. We also wanted to determine if area 3b and 1 quickly adapting (QA) neurons show similar or different activity patterns during the initiation and execution of sensory triggered wrist movements. Four monkeys were trained to make wrist flexion and extension movements in response to vibratory stimuli delivered to the handle which the animals used to control the behavioral paradigm. Two fo the four monkeys also made similar wrist movements following visual cues. We found that the premovement activity of QA neurons located in area 1 (but not area 3b) is comprised of a sensory-related component as well as a movement-related component. The magnitude of these individual components differs in relationship to a neuron's receptive field type, the movement direction and the external force imposed on the stimulated forelimb. Premovement activity of area 3b and area 1 QA neurons occurs at the same time prior to movement, regardless of whether visual or vibratory cues are used to trigger wrist movements. This activity occurs at about the same time as others have observed elevations in the threshold for tactile perception, suggesting that premovement activity and changes in sensory responsiveness before movement may be related. These and previous findings are used to construct a model which may predict the firing patterns of SI QA neurons during behavioral tasks. These findings also suggest that areas 3b and 1 may have different roles in processing task-related somatosensory information.

Monkey primary somatosensory cortical activity during the early reaction time period differs with cues that guide movements

“…Transdural penetrations were made daily into postcentral somatosensory areas, as well as precentral motor cortices. Neuronal activity was discriminated by a template-matching Multispike Detector (Alpha Omega Engineering, Nazareth, Israel), was time-stamped relative to the animal's behavior, and was stored in a computer (Nelson 1988;Nelson et al 1991;Lebedev et al 1994). Wrist position was digitized at 100 Hz and stored along with the digital records of neuronal activity.…”

“…Histological sections of the cortex were prepared, and electrode tracks were reconstructed based on the depth of each recording site from the point where the cortical activity was first encountered and the location of the marking lesions (Nelson 1988;Nelson et al 1991). The location of each recording site was subsequently transferred to a photograph of the surface of the recording areas after appropriate scaling.…”

“…The characteristics of vibration-entrained neurons in SI have been studied under a number of conditions (Mountcastle et al 1969;Nelson et al 1991Nelson et al , 2002Lebedev et al 1994;Lebedev and Nelson 1995;Salinas et al 2000;Romo and Salinas 2003). Two classes of SI neurons are thought to play essential roles in the sense of flutter-vibration: the glabrous quickly adapting (QA) neurons and the Pacinian (PC) neurons (Mountcastle et al 1969).…”

“…Vibratory stimuli can be used to guide motor tasks in behaviorally trained monkeys (Nelson et al 1991(Nelson et al , 2002Lebedev et al 1994;Lebedev and Nelson 1995;Salinas et al 2000;Romo and Salinas 2003). Extracellular recordings in task-performing monkeys reveal some taskrelated activity that is vibration-entrained, suggesting that the entrained activity may code functionally significant information conveyed by vibratory inputs.…”

“…The patterns of neuronal activity evoked in SI vary depending on the modality of sensory stimulation. One characteristic discharge pattern is the rhythmic neuronal activity in response to somatic vibratory stimuli (Mountcastle et al 1969;Nelson et al 1991Nelson et al , 2002Lebedev et al 1994;Lebedev and Nelson 1995;Salinas et al 2000;Romo and Salinas 2003). To some extent, vibration-entrained activity reflects the frequency of vibratory inputs, although some SI neurons may be sensitive to lower frequencies while others are sensitive to higher frequencies.…”