Functional Properties of Primate Putamen Neurons During the Categorization of Tactile Stimuli

Abstract

We used psychometric techniques and neurophysiological recordings to study the role of the putamen in somesthetic perception. Four monkeys were trained to categorize the speed of moving tactile stimuli. Animals performed a task in which one of two target switches had to be pressed with the right hand to indicate whether the speed of probe movement across the glabrous skin of the left, restrained hand was low or high. During the task we recorded the activity of neurons in the putamen contralateral (right) and ipsilateral (left) to the stimulated hand. We found different types of neuronal responses, all present in the right and left putamen. Some neurons responded during the stimulus period, others responded during the hand-arm movement used to indicate categorization, and others responded during both of these periods. The responses of many neurons did not vary either with the speed of the stimuli or in relation to the categorization process. In contrast, neurons of a particular type responded differentially: their activity reflected whether stimulus speed was low or high. These differential responses occurred during the stimulus and hand-arm motion periods. A number of the nondifferential and differential neurons were studied when the same stimuli used in the categorization task were delivered passively. Few neurons with nondifferential discharges, and none of the differential neurons, responded in this condition. In a visually cued control task we studied the possibility that the differential responses were associated with the intention to press or with the trajectory of the hand to one of the target switches. In this condition, a light turned on instructed the animal which target switch to press for a reward. Very few neurons in both hemispheres maintained the differential responses observed during the categorization task. Those neurons that discharged selectively for low or high speeds were analyzed quantitatively to produce a measure comparable with the psychometric function. The thresholds of the resulting neurometric curves for the neuronal populations were very similar to the psychometric thresholds. The activity of a large fraction of these neurons could be used to accurately predict whether the stimulus speed was low or high. The results indicate that the putamen, both contralateral and ipsilateral to the stimulated hand, contains neurons that discharge in response to the somesthetic stimuli during the categorization task. Those neurons that respond irrespective of the stimulus speed appear to be involved in the general sensorimotor behavior of the animal during the execution of the task. The results suggest that the putamen may play a role in bimanual tasks. The recording of neurons in the right and left putamen whose activities correlate with the speed categories suggests that this region of the basal ganglia, in addition to its role in motor functions, is also involved in the animal's decision process.

Discrimination in the Sense of Flutter: New Psychophysical Measurements in Monkeys

“…This differential activity actually was observed only during the comparison stimuli, which would be expected if animals based their decisions exclusively on the second stimulus. Similar responses have been recorded from monkeys trained to categorize the speed of tactile motion on the basis of a single stimulus; some neurons from M1 cortex (E. Salinas and R. Romo, unpublished results), the supplementary motor area (Romo et al, 1993, and the putamen (Romo et al, 1995;Merchant et al, 1997) reflect the sensory decision process in their activity. Werner (1980) has clearly stated the distinctions between the different questions that can be asked about the magnitude of a sensation.…”

Subsecond Timing in Primates: Comparison of Interval Production Between Human Subjects and Rhesus Monkeys

“…These findings suggest, first, that both primate species have a similar internal timing mechanism when the passage of time needs to be quantified for only one interval. Indeed, rhesus monkeys have practically the same abilities as those of humans in a large number of sensorimotor tasks, such as reaching (Georgopoulos et al 1982;Merchant et al 2004a;Naselaris et al 2006), categorizing and discriminating stimuli (Britten et al 1992;Fortes et al 2004;Hernandez et al 1997;Merchant et al 1997;Romo et al 1996), and anticipatory pursuit (Heinen et al 2005;Janssen and Shadlen 2005;Kowler 1989). Furthermore, the interception skills of monkeys are as good as-or even better than-those of human subjects (Merchant et al 2003).…”

Conversion of Sensory Signals into Motor Commands in Primary Motor Cortex

“…The study was performed on four male monkeys, Macaca mulatta, 4.5-6 kg. The task and related procedures are similar to those described previously by Romo et al (1996Romo et al ( , 1997 and Merchant et al (1997). The monkey sat on a primate chair with its head fixed.…”

“…In separate sessions, these and additional muscles from the shoulder, neck and trunk were also recorded, along with activity from the forearm and arm muscles of the left side. Muscles ipsilateral to the responding arm studied in these extra sessions were the anterior and lateral deltoids, the thoracic paraspinal, and the suprascapular and infrascapular trapezius (see Merchant et al, 1997, their Fig. 2).…”

“…A decoding method is a particular recipe to combine the N rates with previous knowledge about the firing statistics of the neurons to generate x est . Signal detection theory has been used previously to compare psychophysical behavior and e xpected behavior-x est is never actually computed-based on the optimal processing of individual neuronal responses (Britten et al, 1992;Thompson et al, 1996;Merchant et al, 1997;Romo et al, 1997). We chose decoding techniques instead because they provide, on a trial by trial basis, a real construct that, unlike the signal detection method, is not limited to single neurons and can be applied to neuronal populations.…”