Tactile activity in primate primary somatosensory cortex during active arm movements: correlation with receptive field properties

Abstract

1. Five hundred ninety-five single neurons with tactile receptive fields (RFs) on the contralateral arm were isolated in the primary somatosensory cortex (SI) of awake, behaving monkeys. 2. Fifty-eight percent of the tactile cells showed significantly different levels of activity during active movements of the arm in eight directions or during active maintenance of the arm over the target endpoints. 3. The discharge of many of the active tactile cells was unimodally tuned with movement direction and the pattern of the tactile population activity varied in a meaningful fashion with arm movement direction and posture. 4. The intensity of the arm-movement-induced activity was typically less than that evoked by direct tactile stimulation of the cell's RF. 5. The probability of task-related activity was correlated with certain RF properties, in particular the sensitivity of the cell to lateral stretch of the skin and to passive arm movements that avoided direct contact of the RF on any surface. 6. This suggests that task-related activity results mainly from the activation of tactile receptors by mechanical deformation of the skin as the arm changes geometry during movement. 7. These results demonstrate that tactile activity containing potential proprioceptive information is generated in SI during active arm movements that avoid direct contact of the skin with external surfaces. Whether or not this input contributes to the kinesthetic sensations evoked by the movements cannot be resolved by this study.

Responses of somatosensory area 2 neurons to actively and passively generated limb movements

“…It is important to note that the limitations of our experimental paradigm did not allow us to reconstruct a forward model fully. Although we and others have described various characteristics of the representation of force and position and its derivatives (Weber et al 2011;Gardner and Costanzo 1981;Prud'homme and Kalaska 1994), we do not know the particular combination of kinematic and dynamic variables that are represented. It is possible to predict other features that might be found if S1 were to represent a Kalman filter.…”

“…Our manipulandum did not constrain all the degrees of freedom of the arm the way the exoskeleton design can; however, this lack of constraint allowed the monkey to make movements that were closer to a natural reach. Additionally, since it is known that cutaneous receptors on the limb can encode limb movement kinematics (Cohen et al 1994;Weber et al 2011), our manipulandum avoided cutaneous stimulation to the proximal limb beyond what would be expected from a natural arm movement. The handle of the manipulandum was allowed to pivot about a vertical axis on low friction bearings to avoid variable cutaneous stimulation to the palm due to slip of the hand across the surface of the handle.…”

“…As in the motor cortex, S1 discharge is sinusoidally tuned to movement direction (Prud'homme and Kalaska 1994). It is convenient to summarize this spatial tuning in terms of the direction of motion to which a neuron responds most strongly, referred to as the "preferred direction" (PD) of the neuron.…”

Population Computation of Vectorial Transformations

“…However, not all distributions are uniform (Hubel & Wiesel, 1962;Oyster & Barlow, 1967;van Gisbergen, van Opstal, & Tax, 1987;Cohen, Prud'homme, & Kalaska, 1994;Lacquaniti et al, 1995;Rosa & Schmid, 1995;Wylie et al, 1998), and it remained to be checked if these distributions are regular. A particular distribution is a clustering of PAs along preferred axes (Oyster & Barlow, 1967;Cohen et al, 1994;Lacquaniti et al, 1995;Wylie et al, 1998; see also Soechting & Flanders, 1992). Populations of neurons in posterior parietal cortex of monkeys have such a distribution of PAs and satisfy the regularity condition (p < 0.01, unpublished observations from the data of Battaglia-Mayer et al, 2000).…”

Where Is Your Arm? Variations in Proprioception Across Space and Tasks

“…Mechanoreceptors in the hairy nonglabrous skin of the hand (Edin 1992;Abbs 1991), ankle (Aimonetti et al 2007), and thigh (Edin 2001) are activated by movements at nearby joints that result in skin stretch. Cells in the primary somatosensory cortex of monkeys discharge in meaningful patterns, depending on arm movement direction and posture, and the sensitivity of these cortical cells to skin stretch is correlated with how well they encode position information (Cohen et al 1994). Experiments also show that different skin stretch patterns affect the perception of finger, elbow, and knee position and movement (Collins and Prochazka 1996;Collins et al 2005;Edin and Johansson 1995).…”