Comparison of neuronal firing rates in somatosensory and posterior parietal cortex during prehension

To evaluate their functional roles during prehension, single-unit recordings were made in the hand area of primary somatosensory areas 3b, 1 and 2 (S-I) and posterior parietal areas 5 and 7 (PPC) of the same animal. Response profiles of mean firing rate during performance of a multistage reach, grasp, and lift task were analyzed to determine the period(s) of peak firing and to measure statistically significant rises or falls in rate compared with baseline. We used the peak firing stage(s) to subdivide the population into classes tuned to single actions or two successive stages, or into multiaction groups that had sustained facilitation (BT) or inhibition (GI) during hand-object interactions. Four times as many neurons fired at peak rates during acquisition stages (approach, contact, grasp) than upon release, and their firing rates were higher. Grasping evoked the strongest responses, as grasp-tuned neurons had the highest peak rates in the population; BT, contact-grasp, and grasp-lift cells also fired maximally in the grasp stage. Grasping also coincided with maximal inhibition of GI cells, as well as of neurons tuned to approach or relaxation of grasp. Holding evoked the lowest mean rates, and had the fewest tuned cells. S-I and PPC showed significant differences in behaviors evoking peak firing as well as facilitation and inhibition; these correlated with input modalities in each area. Hand contact with the object and positioning of the fingers for grasp was the most strongly represented behavior in anterior S-I, where 61% received tactile inputs from glabrous skin. Nearly 60% were facilitated at contact, 38% fired at peak rates, and 10% were inhibited; release of grasp evoked peak firing in only 5% of 3b-1 neurons. In posterior S-I, where proportions of tactile and deep inputs were similar, positioning and grasping elicited peak responses in 38% and 31%, respectively; 80% were facilitated or inhibited during grasping. During lift and hold, inhibition rose to 43%, while excitation declined under 10%. PPC had the highest proportions firing at peak rates during hand preshaping before contact (28%) and had the most facilitated responses (38%) in this stage. Only 10% fired at peak rates during grasping. During later manipulatory actions, proportions of facilitated and inhibited responses in PPC were similar to those in posterior S-I. The data support models in which PPC plans hand movements during prehension rather than guiding their execution. Sensory monitoring of hand-object interaction occurs in S-I, where cells sense specific hand behaviors, signal stage completion, enable error correction, and may update grasp programs formulated in PPC. The results are discussed in relation to those obtained from lesion studies in humans. Electronic Publication     

Activation of respiratory afferents by resistive loaded breathing modifies somatosensory evoked potentials to median nerve stimulation in humans

The cortical projections of respiratory afferents (vagus and respiratory muscle nerves) are well documented in humans. It is also shown that their activation during loaded breathing modifies the perception of tactile sensation as well as the motor drive to skeletal muscles. The effects of expiratory or inspiratory loaded breathing on somatosensory evoked potentials (SEPs) elicited by median nerve stimulation were studied in eight healthy subjects. No significant changes occurred in latencies of N20, N30 and P40 throughout the expiratory loading period, except for a significant lengthening in P1 latency compared with unloaded breathing. However, inspiratory loading induced a significant increase in peak latency of N20, N30 and P40 components. We suggest that projections of inspiratory afferents from the diaphragm and the intercostal muscles, activated by inspiratory loading, could be responsible for the lengthened latency of median nerve SEP components. Thus, respiratory afferents very likely interact with pathways of the somatosensory system.     

Depression of neuronal firing rates in somatosensory and posterior parietal cortex during object acquisition in a prehension task

Prehension is an object-oriented behavior consisting of four components: reach, grasp, manipulation, and release. To determine how such actions are represented in primary somatosensory (S-I) and posterior parietal cortex (PPC), we used digital video to synchronize spike trains of neurons recorded in Brodmann's areas 3b, 1, 2, 5, and 7 with the hand kinematics as monkeys performed a prehension task. Statistical analyses indicated that one-third of task-modulated neurons showed significantly depressed firing rates during object acquisition and/or manipulation. This population was dominated by neurons innervated by deep receptors that sensed extension movements of the fingers, or by tactile receptors in hairy skin sensing stretch. Grasp-inhibited responses were the most common type. Tonic firing rates of these cells dropped significantly during approach as the hand was preshaped for grasping, or at contact when grasp was initiated, and persisted until hand motion ceased or as the grip relaxed. Maximum suppression of firing occurred at grasp completion. Their lack of specificity for particular hand behaviors formed the inhibitory counterpart of broadly tuned cells that fired prolonged bursts during grasp and manipulatory stages of prehension. The remainder of the task-inhibited population showed biphasic responses. Firing rates were significantly depressed during grasping and manipulation when the hand interacted directly with the object, but were enhanced prior to contact, when the hand was preshaped (approach-tuned), or upon relaxation of grasp and release of the object from the hand (loweror relax-tuned). Grasp-inhibited responses occurred primarily in S-I, whereas biphasic inhibitory activity was recorded mainly in PPC. Suppression of activity within these populations may thereby increase the saliency of excitatory responses to acquisition and manipulation of objects. Reduction of firing during prehension might also signal the flexed postures used to retain objects in the hand, rather than a generalized gating of sensory information. The similarity of responses to active and passive extension movements suggests that the inhibitory responses may provide important postural and motor information about the hand kinematics when performing skilled tasks.     

Functional properties of neurones in the parietal retroinsular cortex in awake monkey

The parietal retroinsular cortex of three, awake, behaving macaque monkeys was investigated using transdural microelectrode recording technique. All 73 cells identified responded to somatosensory stimuli. Most of the neurones (51) were activated by compression of the skin in an on, off or on-off fashion; these cells were unresponsive to light touching or stroking of the skin. The rest of the cells responded to light touching, rotation of a joint or palpation of a muscle belly. All body parts were represented in this area. Of the cells 30% responded to stimulation of both sides of the body. The results indicate that the parietal retroinsular cortex participates in the analysis of skin compression. This information is used, i.e. in the control of manipulative movements and in discrimination of supported weights. It is possible that ablation of the area examined would impair these functions.     

Saccade and blinking evoked by microstimulation of the posterior parietal association cortex of the monkey

Summary Electrical stimulation with microelectrodes of the posterior parietal association cortex in alert behaving monkeys elicited saccadic eye movements and blinking. The sites in which saccades were elicited by electrical stimulation were concentrated in the anteromedial part of area 7a, especially in the posterior bank of the intraparietal sulcus, in a region which sends efferent projections to the frontal eye field and the superior colliculus, but they were also found in the posterolateral part of area 7a. Compared with the frontal eye fields and the superior colliculus, the threshold current for eliciting saccades was relatively high, on the average 86 A. Moreover, the elicitation of saccade was inconsistent even with suprathreshold stimulation and suppressed during visual fixation. Latencies of the saccades were relatively long, on the average 50 ms; they were longer in the posterolateral part than in the anteromedial part. Direction and amplitude of evoked saccades depended on the site of stimulation, but was independent of eye position in most cases. However, goal-directed saccades which depended on initial eye position were elicited in three penetrations in the posterolateral part of area 7a. Blinking was elicited mainly in the lateral part of area 7a. The threshold of blinking was 70 A and the latency was 50 ms on the average. In contrast to saccades, blinking was elicited constantly with each stimulus even during attentive fixation. We occasionally recorded single unit activity at the site of stimulation with the same electrodes. More than half of the units recorded at the site of blinking responded to approaching visual stimulus. These results suggest that area 7a participates indirectly in the control of saccades by way of its connection to the frontal eye fields or the superior colliculus, and it may also play an important role in blinking in response to a visual threat.Prof. J. Hyvärinen died on February 26, 1983     

Facilitation of neuronal activity in somatosensory and posterior parietal cortex during prehension

In order to study prehension in a reproducible manner, we trained monkeys to perform a task in which rectangular, spherical, and cylindrical objects were grasped, lifted, held, and lowered in response to visual cues. The animal’s hand movements were monitored using digital video, together with simultaneously recorded spike trains of neurons in primary somatosensory cortex (S-I) and posterior parietal cortex (PPC). Statistically significant task-related modulation of activity occurred in 78% of neurons tested in the hand area; twice as many cells were facilitated during object acquisition as were depressed. Cortical neurons receiving inputs from tactile receptors in glabrous skin of the fingers and palm, hairy skin of the hand dorsum, or deep receptors in muscles and joints of the hand modulated their firing rates during prehension in consistent and reproducible patterns. Spike trains of individual neurons differed in duration and amplitude of firing, the particular hand behavior(s) monitored, and their sensitivity to the shape of the grasped object. Neurons were classified by statistical analysis into groups whose spike trains were tuned to single task stages, spanned two successive stages, or were multiaction. The classes were not uniformly distributed in specific cytoarchitectonic fields, nor among particular somatosensory modalities. Sequential deformation of parts of the hand as the task progressed was reflected in successive responses of different members of this population. The earliest activity occurred in PPC, where 28% of neurons increased firing prior to hand contact with objects; such neurons may participate in anticipatory motor control programs. Activity shifted rostrally to S-I as the hand contacted the object and manipulated it. The shape of the grasped object had the strongest influence on PPC cells. The results suggest that parietal neurons monitor hand actions during prehension, as well as the physical properties of the grasped object, by shifting activity between populations responsive to hand shaping, grasping, and manipulatory behaviors. Received: 1 October 1998 / Accepted: 4 May 1999     

Somatotopic organization of the human somatosensory cortex revealed by neuromagnetic measurements

Summary The primary projection areas in the human somatosensory cortex activated by electrical stimulation of the digits of the hand and the ankle were localized by measuring the magnetic field outside the head contralateral to the side of stimulation. Most of the spatial variation in the amplitude of the field component normal to the scalp could be accounted for by representing each source as a single current dipole in a spherical conducting medium with solely concentric variations in electrical conductivity, although the fit of this model to the data showed some statistically significant deviations. Based on the best-fitting parameter values of the model, we found that the projection areas of the thumb, the index finger, the little finger and the ankle were located at successively more medial positions along the primary somatosensory cortex, at an average depth of 2.2 cm from the scalp surface.This research was supported in part by ONR grant N00014-76-C-0568The preliminary results from the present study were reported at the Sixth Conference on Slow Potentials in the Human Brain held in 1981 (Kaufman et al. 1984) and at the Fourth Workshop on Biomagnetism held in 1982 (Okada 1983)     

Effects of repetitive transcranial magnetic stimulation over dorsolateral prefrontal and posterior parietal cortex on memory-guided saccades

We investigated the role of the dorsolateral prefrontal cortex (DLPFC) and the posterior parietal cortex (PPC) in a visuospatial delayed-response task in humans. Repetitive transcranial magnetic stimulation (20 Hz, 0.5 s) was used to interfere temporarily with cortical activity in the DLPFC and PPC during the delay period. Omnidirectional memory-guided saccades with a 3-s delay were used as a quantifiable motor response to a visuospatial cue. The question addressed was whether repetitive transcranial magnetic stimulation (rTMS) over the DLPFC or PPC during the sensory of memory phase affects accuracy of memory-guided saccades. Stimulation over the primary motor cortex served as control. Stimulation over the DLPFC significantly impaired accuracy of memory-guided saccades in amplitude and direction. Stimulation over the PPC impaired accuracy of memory-guided saccades only when applied within the sensory phase (50 ms after cue offset), but not during the memory phase (500 ms after cue offset). These results provide further evidence for a parieto-frontal network controlling performance of visuospatial delayed-response tasks in humans. It can be concluded that within this network the DLPFC is mainly concerned with the mnemonic respresentation and the PPC with the sensory representation of spatially defined perceptual information. Received: 22 April 1996/Accepted: 16 June 1997     

Mixed and sensory nerve stimulations activate different cytoarchitectonic areas in the human primary somatosensory cortex SI

Summary Magnetic responses evoked by stimulation of the mixed median nerve at the wrist and its cutaneous branches on the glabrous skin of the index and middle fingers were studied. The first responses to mixed nerve stimulation peaked at 19–24 ms, and those to cutaneous nerve stimulation about 4 ms later. The responses, up to a latency of 150 ms, reversed in polarity between the upper and lower parts of the rolandic fissure. Equivalent dipoles for the mixed nerve stimulation were stronger and they lay statistically significantly deeper from the scalp than those activated by the cutaneous nerve stimulation. It is suggested that mixed nerve stimulation activates areas 3a and 3b whereas cutaneous stimulation activates mainly area 3b at the human primary somatosensory cortex. Statistical procedures were developed for comparison of different field patterns and for determining confidence limits of source model parameters. For these purposes the quality and quantity of the noise were studied. The error caused by inaccuracies in the positioning of the magnetometer was found to be minimal in comparison with the signal noise which was estimated from the standard deviation of the averaged response.     

Responses of the human auditory cortex to changes in one versus two stimulus features

Neuromagnetic responses were recorded with a 24 SQUID magnetometer in two oddball experiments to determine whether mismatch responses to changes in single stimulus features are additive. In experiment 1, the one feature deviants differed from standards in interstimulus interval (ISI) or frequency, and the two feature deviants in both ISI and frequence. In experiment 2, deviants differed in duration, frequency, or both. All deviants evoked a mismatch field (MMF) with sources close to each other in the supratemporal auditory cortex. Except for the ISI deviants, the MMF sources were about 1 cm anterior to the source of the 100ms response, N100m, to the standards. In the two experiments, MMFs obtained in response to the two feature deviants resembled closely the sum of MMFs in response to one feature deviants. The results suggest that the standards leave a multiple neuronal representation in the human auditory cortex. The particular neuronal traces of the representation react independently to changes in different features of sound stimuli.     

Electrical microstimulation of primate posterior parietal cortex initiates orienting and alerting components of covert attention

The posterior parietal cortex (PPC) is implicated in the control of visuospatial orienting, including both overt saccadic eye movements and covert shifts of attention (i.e., attention to a location other than at visual fixation). Some studies have suggested that the attentional system is part of the premotor processing in the brain, while others suggest they are separate. Here, we test how the PPC controls covert attention shifts in the absence of executed eye movements. Electrical microstimulation was applied to the right PPC while monkeys performed a spatial, cued target detection task, in which they were not allowed to move their gaze. At high currents, contralateral saccades were evoked. With currents below the thresholds for eliciting saccades, microstimulation produced a purely attentional shift (as indexed by decreased target reaction time) when a cue and target were presented in the contralateral visual field. This suggests that microstimulation can move attention specifically in the absence of any overt movements of the eyes or limbs. In addition, there was a reduction in reaction times in trials that did not evoke attentional orienting, suggesting a more general alerting effect of microstimulation These data provide direct evidence that the PPC may be a source of both attentional modulation of neuronal responses and saccadic eye movements to peripheral visual stimuli.     

Functional clusters in the human parietal cortex as revealed by an observer-independent meta-analysis of functional activation studies

The human parietal cortex is a highly differentiated structure consisting of cytoarchitectonically defined subareas that are specifically connected with other cortical and subcortical areas. Based on evidence from neurophysiological studies in subhuman primates these subareas are supposed to be functionally highly specialized. Here, we reviewed 51 different neuroimaging studies on healthy subjects with activation of the parietal lobe in statistical parametric maps. Running a cluster analysis on the stereotactic coordinates of the centers of gravity of the activation areas and plotting them into Talairach space showed a high consistency of the mean activation foci for similar paradigms across different laboratories and functional imaging modalities. Our meta-analysis exposed seven distinct pairs of quite symmetrically distributed subareas of the parietal cortex of each hemisphere as well as three unpaired regions that are critically involved in the generation of limb and eye movements in egocentric and allocentric coordinates, but also in attention, memory and cognitive problem solving. These data highlights the modular organization of the human parietal lobe. By its locally interspersed distributed circuits it orchestrates specialized cognitive subfunctions interfacing perception and action. Our meta-analysis provides a new framework for understanding information processing in the human parietal cortex.     

Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey

We studied the functional properties of rotation-sensitive (RS) neurons of the posterior parietal association cortex in detail. We classified 58 neurons as RS neurons on the basis of statistical analysis, to indicate that their responses to rotary movement were significantly greater (P<0.01) than those to linear movement of the same stimulus. We calculated rotation index, 1 — (L/R), in 82 cells, where L/R is the ratio of net response to linear movement to that to rotary movement. All the RS neurons had rotation index greater than or equal to 0.3. The recording site of these RS neurons was localized in the posterolateral part of area PG (area 7a of Vogt), on the anterior bank of the caudal superior temporal sulcus (STS), in the region partly overlapping the medial superior temporal (MST) area. We compared the response of RS neurons to rotation with that to shearing movement as well as to linear movement. In the majority of RS neurons the ratio of shearing response to rotation response (S/R) was smaller than the ratio of linear response to rotation response (L/R), indicating that the response to rotation was not due to a simple combination of linear movements in the opposite direction. Most of the RS neurons responded to the rotary movement of a single spot as well as that of a slit, although the response was smaller (average 70%) for the former. Most of the RS neurons had large receptive fields (60–180° in diameter) and their responses were independent of the position within the receptive field. The responses of most RS neurons increased monotonically with the increase in angular velocity and were also dependent on the size of the stimulus, although the rate of increase was small when the length was more than 10°. The majority of RS neurons (37/58) responded better to rotation in depth than to that in the frontoparallel plane. Some of them (12/37) responded to diagonal rotation rather than to sagittal or horizontal rotation. We found that some depth RS neurons showed reversal in the preferred direction when we used a trapezoidal window-like plate as the rotating stimulus in the monocular viewing condition, just as occurs in the case of the Ames window illusion. The response of some RS neurons (5/7) was enhanced by tracking eye movement. The enhanced responses were observed during rotary tracking but not during linear tracking. Other RS neurons (n = 2) showed maximum response to the rotation of the monkey chair in the light, as a result of convergence of visual and vestibular signals. We concluded that the continuous change of direction of movement was the most important cue for RS neurons to respond selectively to rotary movement in contrast to linear translational movement, and that these neurons were likely to discriminate the direction and orientation of the plane of rotation of the object in space.     

Characterization of the human auditory cortex by the neuromagnetic method

Summary Neuromagnetic studies show that the location of cortical activity evoked by modulated tones and by click stimuli in the steady state paradigm can be determined non-invasively with a precision of a few millimeters. The progression of locations for tones of increasing frequency establish an orderly tonotopic map in which the distance along the cortex varies as the logarithm of the frequency. The active region responding to clicks lies at a position that is consistent with this map if the stimulus is characterized by the frequency of the peak of its power spectrum. A latency of about 50 ms observed for the response to clicks is in close correspondance with a strong component of the transient response to an isolated click reported in the literature. Monaural stimulation of the ear contralateral to the hemisphere being monitored produces a latency which is about 8 ms shorter than stimulation of the ipsilateral ear, in agreement with previous studies of transient responses. The amplitudes of the responses for binaurally presented clicks for sleeping subjects is substantially diminished for repetition rates above 20 Hz but is enhanced for lower rates.Supported in part by Office of Naval Research Contract N00014-76-C-0568Supported by Consiglio Nazionale delle Ricerche and by Progetto Finalizzato Superconduttivitá — C.N.R.     

Subregions of human parietal cortex selectively encoding object orientation

Computation of object orientation could be an independent process from those of other object features, but currently neither the location of human brain areas selectively coding orientation information nor an optimum experimental paradigm have yet been established. In this study, functional magnetic resonance imaging was used to investigate brain activation in the parietal cortices related to object orientation. Using an Arabic digit whose spatial attributes were carefully manipulated, we found parietal areas exclusively sensitive to object orientation, but not to general spatial attention. It seems that, by excluding confounds such as mental manipulation or working memory as well as inherent spatial information within the stimuli, functional segregation within the parietal lobe can be effectively probed.     

Memory related motor planning activity in posterior parietal cortex of macaque

Summary Unit recording studies in the lateral bank of the intraparietal cortex (area LIP) have demonstrated a response property not previously reported in posterior cortex. Studies were performed in the Rhesus monkey during tasks which required saccadic eye movements to remembered target locations in the dark. Neurons were found which remained active during the time period for which the monkey had to withhold eye movements while remembering desired target locations. The activity of the cells was tuned for eye movements of specific direction and amplitude, and it was not necessary for a visual stimulus to fall within the response field. The responses appeared to represent a memory-related motor-planning signal encoding motor error. The relation of the activity to the behavior of the animal suggests that the response represents the intent to make eye movements of specific direction and amplitude.     

Responses of the human auditory cortex to vowel onset after fricative consonants

Summary Neuromagnetic responses to different auditory stimuli (noise bursts and short speech stimuli) were mapped over both hemispheres of seven healthy subjects. The results indicate that a particular acoustic feature of speech, vowel onset after voice-less fricative consonants, evokes a prominent response in the human supratemporal auditory cortex. Although the observed response seems to be specific to acoustic rather than phonetic characteristics of the stimuli, it might reflect feature detection essential for further speech processing.     

Damage to superior parietal cortex impairs pointing in the sagittal Plane

Neurophysiology and neuroimaging research implicates distinct regions of posterior parietal cortex for reaching versus grasping and for completing these movements in central versus peripheral space. Typically, visuomotor tasks only examine movements made in the frontoparallel plane. We examined a patient with a right superior parietal lesion encompassing the parietal-occipital junction, the intraparietal sulcus and the putative human homologue of V6A on pointing tasks in the sagittal or frontoparallel planes. The patient did not demonstrate a speed-accuracy trade-off, but did show larger times post-peak velocity for all movement directions. Her movements in the sagittal axis were more disordered than movements in the frontoparallel plane. These data indicate a role for superior parietal cortex in fine tuning of visually guided movements and more particularly for movements made back towards the body.

Low frequency rTMS over posterior parietal cortex impairs smooth pursuit eye tracking

The role of the posterior parietal cortex in smooth pursuit eye movements remains unclear. We used low frequency repetitive transcranial magnetic stimulation (rTMS) to study the cognitive and neural systems involved in the control of smooth pursuit eye movements. Eighteen participants were tested on two separate occasions. On each occasion we measured smooth pursuit eye tracking before and after 6 min of 1 Hz rTMS delivered at 90% of motor threshold. Low frequency rTMS over the posterior parietal cortex led to a significant reduction in smooth pursuit velocity gain, whereas rTMS over the motor cortex had no effect on gain. We conclude that low frequency offline rTMS is a potentially useful tool with which to explore the cortical systems involved in oculomotor control.     

The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey

Summary The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey was analyzed using autoradiographic techniques. Posterior parietal fibers are located in the posterior half of the body of the corpus callosum. There is some segregation of fibers with respect to their place of origin within the posterior parietal lobe. However, there is also overlap, particularly between fibers coming from the caudal inferior parietal lobule and the medial parietal lobe.Supported by the Veterans Administration, Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Massachusetts and N.I.H. Grants NS 09211 and NS 16841