Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey

1. Single cell activity was studied in the precentral (PCM), premotor (PM), and supplementary (SMA) motor cortex of the monkey to compare magnitudes of activity changes in relation to ipsilateral, contralateral, and bilateral digit movements. 2. Three Japanese monkeys were trained to press a small key with the right or left hand, or with both hands, in accordance with visual instruction signals given 2.6-5.4 s before a visual movement-trigger signal. Great care was taken to train the animal to use only the required part of the limb. As a result of extensive training, electromyographic (EMG) studies revealed that muscle activities before the key press were limited to the digit and hand muscles of the limb instructed to move. No overt increase or decrease in activity was detectable in the proximal limb or body muscles in relation to the key-press movements or instructions. 3. Even though the movement was thus limited to distal forelimb, distinct ipsilateral relationships were observed in 8.2% of the task-related PCM neurons. They changed their activity before ipsilateral and bilateral (but not before contralateral) key press. 4. A majority of the neurons recorded from the digit area of PCM (mostly limited to the anterior bank of the central sulcus) exhibited a contralateral relationship; namely the activity increased or decreased before the onset of the contralateral and bilateral key-press movements. In most of them, the magnitudes of the activity changes before the contralateral and bilateral movements were similar. 5. In proximal limb and trunk areas of PCM and also in the somatosensory cortex, no neurons were found to exhibit distinct relations to any of the key-press movements. 6. In both SMA and PM, a number of neurons exhibited relationships of the type never or only rarely observed in the primary motor cortex. Thirty-seven percent of SMA and 62% of PM neurons exhibited premovement activity changes before all of the key-press movements. The movement-specific type of activity was observed in 28% of SMA and 16% of PM neurons. In these neurons, the activity changes were observed in relation to only one of the right or left key-press movements or exclusively in relation to the bilateral key press. Neuronal activity resembling the majority of the PCM neurons (contralateral type) was observed in 31% of SMA and 13% of PM neurons. 7. Instruction-induced changes in activity were more often found in the secondary than in the primary motor area.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neuronal activity in motor cortical areas reflects the sequential context of movement

Natural actions can be described as chains of simple elements, whereas individual motion elements are readily concatenated to generate countless movement sequences. Sequence-specific neurons have been described extensively, suggesting that the motor system may implement temporally complex motions by using such neurons to recruit lower-level movement neurons modularly. Here, we set out to investigate whether activity of movement-related neurons is independent of the sequential context of the motion. Two monkeys were trained to perform linear arm movements either individually or as components of double-segment motions. However, comparison of neuronal activity between these conditions is delicate because subtle kinematic variations generally occur within different contexts. We therefore used extensive procedures to identify the contribution of variations in motor execution to differences in neuronal activity. Yet, even after application of these procedures we find that neuronal activity in the motor cortex (PMd and M1) associated with a given motion segment differs between the two contexts. These differences appear during preparation and become even more prominent during motion execution. Interestingly, despite context-related differences on the single-neuron level, the population as a whole still allows a reliable readout of movement direction regardless of the sequential context. Thus the direction of a movement and the sequential context in which it is embedded may be simultaneously and reliably encoded by neurons in the motor cortex.     

Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey

We investigated how neurons in the different motor areas of the frontal lobe reflect the movement dynamics, and how their neuronal activity undergoes plastic changes when monkeys adapt to perturbing forces (they learn new dynamics). Here we describe the results obtained in the dorsal premotor area (PMd) and ventral premotor area (PMv). Monkeys performed visually instructed, delayed reaching movements before, during and after exposure and adaptation to a viscous, curl force field. During movement planning (i.e., during an instructed delay that followed the cue and preceded the go signal), we found dynamics-related activity in PMd but not in PMv. A closer analysis revealed that the population of PMd reflected the dynamics of the upcoming movement increasingly over the course of the delay, starting from a kinematics-related signal. During movement execution, dynamics-related activity was present in both PMd and PMv. In this respect, the results for PMd were similar to that previously found for the supplementary motor area (SMA) whereas the results for PMv were more similar to that previously found for the primary motor cortex (M1). Plastic changes associated with the acquisition of new dynamics found in PMd and PMv were qualitatively similar to those previously observed in M1 and SMA. The ensemble of our experiments suggest a broader picture of the cortical control of movements, whereby multiple areas all contribute to the various sensorimotor processes, including “low” computations such as the movement dynamics, but also express a degree of specialization.     

Connections between the amygdala and auditory cortical areas in the macaque monkey

Connections between the amygdala and auditory cortical areas TC, and the rostral, intermediate and caudal regions of area TA (TAr, TAi and TAc, respectively) in the macaque monkey (Macaca fuscata and Macaca nemestrina) were investigated following placements of cortical deposits of wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). Areas TC and TAc received weak projections and these derived only from the lateral basal nucleus. Areas TAi and TAr received projections from the lateral, lateral basal and accessory basal nuclei. In contrast, corticopetal projections to the amygdala originated in areas TAi and TAr, but never in TAc or TC. The projections from areas TAi and TAr terminated only in the lateral nucleus, and in particular at the lateral part of the middle and caudal portions of the amygdala. Thus, the amygdalofugal projections to the auditory cortices are more widespread and more complex than the amygdalopetal projections of the auditory cortices. As judged from experiments in which deposits were made at different sites along the rostrocaudal axis of the auditory cortex, there was a progressive increase seen in density of the amygdala connections with more anteriorly-placed injection sites.     

Neuronal correlates of conditioned inhibition of the eyeblink response in the anterior interpositus nucleus

Conditioned inhibition (CI) of the rat eyeblink response and the neuronal correlates of CI in the cerebellar interpositus nucleus were examined in the present study. In Experiment 1, CI was established with a novel, 3-group design. In Experiment 2, neuronal activity in the anterior interpositus nucleus was recorded during CI training and testing. Each rat was given 2 training phases and then tested for CI with summation and retardation tests. Rats given CI training showed behavioral inhibition compared with rats in 2 control groups. Neuronal activity in the anterior interpositus nucleus correlated with behavioral responding during discrimination training and during the summation test. The results suggest that neurons in the cerebellar anterior interpositus nucleus may participate in the acquisition or expression of CI.     

Differentiating cortical areas related to pain perception from stimulus identification: temporal analysis of fMRI activity.

In a recent functional magnetic resonance imaging study (fMRI), we reported the cortical areas activated in a thermal painful task and compared the extent of overlap between this cortical network and those activated during a vibrotactile task and a motor task. In the present study we examine the temporal properties of the cortical activations for all three tasks and use linear systems identification techniques to functionally differentiate the cortical regions identified in the painful thermal task. Cortical activity was examined in the contralateral middle third of the brain of 10 right-handed subjects, using echo-planar imaging and a surface coil. In another eight subjects the temporal properties of the thermal task were examined psychophysically. The fMRI impulse response function was estimated from the cortical activations in the vibrotactile and motor tasks and shown to correspond to earlier reports. Given the fMRI impulse response function and the time courses for the thermal stimulus and the associated pain ratings, predictor functions were generated. The correlation between these predictor functions and cortical activations in the painful thermal task indicated a gradual transition of information processing anteroposteriorly in the parietal cortex. Within this region, activity in the anterior areas more closely reflected thermal stimulus parameters, whereas activity more posteriorly was better related to the temporal properties of pain perception. Insular cortex at the level of the anterior commissure was the region best related to the thermal stimulus, and Brodmann's area 5/7 was the region best related to the pain perception. The functional implications of these observations are discussed.     

Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP (the superior temporal polysensory area) of the macaque monkey

Pyramidal neurones were injected with Lucifer Yellow in slices cut tangential to the surface of area 7 m and the superior temporal polysensory area (STP) of the macaque monkey. Comparison of the basal dendritic arbors of supra- and infragranular pyramidal neurones (n = 139) that were injected in the same putative modules in the different cortical areas revealed variation in their structure. Moreover, there were relative differences in dendritic morphology of supra- and infragranular pyramidal neurones in the two cortical areas. Sholl analyses revealed that layer III pyramidal neurones in area STP had considerably higher peak complexity (maximum number of dendritic intersections per Sholl circle) than those in layer V, whereas peak complexities were similar for supra- and infragranular pyramidal neurones in area 7 m. In both cortical areas, the basal dendritic trees of layer III pyramidal neurones were characterized by a higher spine density than those in layer V. Calculations of the total number of dendritic spines in the "average" basal dendritic arbor revealed that layer V pyramidal neurones in area 7 m had twice as many spines as cells in layer III (4535 and 2294, respectively). A similar calculation for neurones in area STP revealed that layer III pyramidal neurones had approximately the same number of spines as cells in layer V (3585 and 3850 spines, respectively). Relative differences in the branching patterns of, and the number of spines in, the basal dendritic arbors of supra- and infragranular pyramidal neurones in the different cortical areas may allow for integration of different numbers of inputs, and different degrees of dendritic processing. These results support the thesis that intra-areal circuitry differs in different cortical areas.     

Own-species bias in the representations of monkey and human face categories in the primate temporal lobe

Face categorization is fundamental for social interactions of primates and is crucial for determining conspecific groups and mate choice. Current evidence suggests that faces are processed by a set of well-defined brain areas. What is the fine structure of this representation, and how is it affected by visual experience? Here, we investigated the neural representations of human and monkey face categories using realistic three-dimensional morphed faces that spanned the continuum between the two species. We found an "own-species" bias in the categorical representation of human and monkey faces in the monkey inferior temporal cortex at the level of single neurons as well as in the population response analyzed using a pattern classifier. For monkey and human subjects, we also found consistent psychophysical evidence indicative of an own-species bias in face perception. For both behavioural and neural data, the species boundary was shifted away from the center of the morph continuum, for each species toward their own face category. This shift may reflect visual expertise for members of one's own species and be a signature of greater brain resources assigned to the processing of privileged categories. Such boundary shifts may thus serve as sensitive and robust indicators of encoding strength for categories of interest.     

Loss of nonphosphorylated neurofilament immunoreactivity in temporal cortical areas in Alzheimer's disease

The distribution of immunoreactive neurons with nonphosphorylated neurofilament protein (SMI32) was studied in temporal cortical areas in normal subjects and in patients with Alzheimer's disease (AD). SMI32 immunopositive neurons were localized mainly in cortical layers II, III, V and VI, and were medium to large-sized pyramidal neurons. Patients with AD had prominent degeneration of SMI32 positive neurons in layers III and V of Brodmann areas 38, 36, 35 and 20; in layers II and IV of the entorhinal cortex (Brodmann area 28); and hippocampal neurons. Neurofibrillary tangles (NFTs) were stained with Thioflavin-S and with an antibody (AT8) against hyperphosphorylated tau. The NFT distribution was compared to that of the neuronal cytoskeletal marker SMI32 in these temporal cortical regions. The results showed that the loss of SMI32 immunoreactivity in temporal cortical regions of AD brain is paralleled by an increase in NFTs and AT8 immunoreactivity in neurons. The SMI32 immunoreactivity was drastically reduced in the cortical layers where tangle-bearing neurons are localized. A strong SMI32 immunoreactivity was observed in numerous neurons containing NFTs by double-immunolabeling with SMI32 and AT8. However, few neurons were labeled by AT8 and SMI32. These results suggest that the development of NFTs in some neurons results from some alteration in SMI32 expression, but does not account for all, particularly, early NFT-related changes. Also, there is a clear correlation of NFTs with selective population of pyramidal neurons in the temporal cortical areas and these pyramidal cells are specifically prone to formation of paired helical filaments. Furthermore, these pyramidal neurons might represent a significant portion of the neurons of origin of long corticocortical connection, and consequently contribute to the destruction of memory-related input to the hippocampal formation.     

Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements

To study how neurons in the medial motor areas participate in performing sequential multiple movements that are individually separated in time, we analyzed neuronal activity in the supplementary (SMA) and presupplementary (pre-SMA) motor areas. Monkeys were trained to perform three different movements separated by waiting times, in four or six different orders. Initially each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order without the visual signals. Three types of neuronal activity were of particular interest; these appeared to be crucially involved in sequencing the multiple motor tasks in different orders. First, we found activity changes that were selective for a particular sequence of the three movements that the monkeys were prepared to perform. The sequence-selective activity ceased when the monkeys initiated the first movement. Second, we found interval-selective activity that appeared in the interval between one particular movement and the next. Third, we found neuronal activity representing the rank order of three movements arranged chronologically; that is, the activity differed selectively in the process of preparing the first, second, or third movements in individual trials. The interval-selective activity was more prevalent in the SMA, whereas the rank-order selective activity was more frequently recorded in the pre-SMA. These results suggest how neurons in the SMA and pre-SMA are involved in sequencing multiple movements over time.     

A stereological approach to human cortical architecture: identification and delineation of cortical areas

Stereology offers a variety of procedures to analyze quantitatively the regional and laminar organization in cytoarchitectonically defined areas of the human cerebral cortex. Conventional anatomical atlases are of little help in localizing specific cortical areas, since most of them are based on a single brain and use highly observer-dependent criteria for the delineation of cortical areas. In consequence, numerous cortical maps exist which greatly differ with respect to number, position, size and extent of cortical areas. We describe a novel algorithm-based procedure for the delineation of cortical areas, which exploits the automated estimation of volume densities of cortical cell bodies. Spatial sampling of the laminar pattern is performed with density profiles, followed by multivariate analysis of the profiles' shape, which locates the cytoarchitectonic borders between neighboring cortical areas at sites where the laminar pattern changes significantly. The borders are then mapped to a human brain atlas system comprising tools for three dimensional reconstruction, visualization and morphometric analysis. A sample of brains with labeled cortical areas is warped into the reference brain of the atlas system in order to generate a population map of the cortical areas, which describes the intersubject variability in spatial conformation of cortical areas. These population maps provide a novel tool for the interpretation of images obtained with functional imaging techniques.     

Differential characteristics of face neuron responses within the anterior superior temporal sulcus of macaques

The anterior superior temporal sulcus (STS) of macaque monkeys is thought to be involved in the analysis of incoming perceptual information for face recognition or identification; face neurons in the anterior STS show tuning to facial views and/or gaze direction in the faces of others. Although it is well known that both the anatomical architecture and the connectivity differ between the rostral and caudal regions of the anterior STS, the functional heterogeneity of these regions is not well understood. We recorded the activity of face neurons in the anterior STS of macaque monkeys during the performance of a face identification task, and we compared the characteristics of face neuron responses in the caudal and rostral regions of the anterior STS. In the caudal region, facial views that elicited optimal responses were distributed among all views tested; the majority of face neurons responded symmetrically to right and left views. In contrast, the face neurons in the rostral region responded optimally to a single oblique view; right-left symmetry among the responses of these neurons was less evident. Modulation of the face neuron responses according to gaze direction was more evident in the rostral region. Some of the face neuron responses were specific to a certain combination of a particular facial view and a particular gaze direction, whereas others were associated with the relative spatial relationship between facial view and gaze direction. Taken together, these results indicated the existence of a functional heterogeneity within the anterior STS and suggested a plausible hierarchical organization of facial information processing.     

Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey

1. We examined the sensory properties of cells in the anterior bank of the caudal part of the superior temporal sulcus (caudal STS) in anesthetized, paralyzed monkeys to visual, auditory, and somesthetic stimuli. 2. In the anterior bank of the caudal STS, there were three regions distinguishable from each other and also from the middle temporal area (MT) in the floor of the STS and area Tpt in the superior temporal gyrus. The three regions were located approximately in the respective inner, middle, and outer thirds of the anterior bank of the caudal STS. These three regions are referred to, from the inner to the outer, as the medial superior temporal region (MST), the mostly unresponsive region, and the caudal STS polysensory region (cSTP), respectively. 3. The extent of MST and its response properties agreed with previous studies. Cells in MST responded exclusively to visual stimuli, had large visual receptive fields (RFs), and nearly all (91%) showed directional selectivity. 4. In the mostly unresponsive region, three quarters of cells were unresponsive to any stimulus used in this study. A quarter of the cells responded to only visual stimuli and most did not show directional selectivity for moving stimuli. Several directionally selective cells responded to movements of three-dimensional objects, but not of projected stimuli. 5. The response properties of cells in the superficial cortex of the caudal superior temporal gyrus, a part of area Tpt, external to cSTP were different from those of cells in the three regions in the anterior bank of the STS. Cells in Tpt were exclusively auditory, and had much larger auditory RFs (mean = 271 degrees) than those of acoustically-driven cSTP cells (mean = 138 degrees). 6. The cSTP contained unimodal visual, auditory, and somesthetic cells as well as multimodal cells of two or all three modalities. The sensory properties of cSTP cells were as follows. 1) Out of 200 cells recorded, 102 (51%) cells were unimodal (59 visual, 33 auditory, and 10 somesthetic), 36 (18%) cells were bimodal (21 visual+auditory, 7 visual+somesthetic, and 8 auditory+somesthetic), and four (2%) cells were trimodal. Visual and auditory responses were more frequent than somesthetic responses: the ratio of the population of cells driven by visual: auditory: somesthetic stimuli was 3:2:1. 2) Visual RFs were large (mean diameter, 59 degrees), but two-thirds were limited to the contralateral visual hemifield. About half the cells showed directional selectivity for moving visual stimuli. None showed selectivity for particular visual shapes.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey

The amygdala has been implicated in processing information about the emotional significance of the environment and in the expression of emotions, through robust pathways with prefrontal, anterior temporal areas, and central autonomic structures. We investigated the anatomic organization and intersection of these pathways in the amygdala in rhesus monkeys with the aid of bidirectional, retrograde and anterograde tracers. Connections of the amygdala with orbitofrontal and medial prefrontal areas were robust and bidirectional, whereas connections with lateral prefrontal areas were sparse, unidirectional and ascending. Orbitofrontal axons terminated densely in a narrow band around the borders of the magnocellular basolateral nucleus, surrounded by projection neurons along a continuum through the nuclei of the basal complex. In contrast, the input and output zones of medial prefrontal areas were intermingled in the amygdala. Moreover, medial prefrontal axonal terminations were expansive, spreading into the parvicellular basolateral nucleus, which is robustly connected with hypothalamic autonomic structures, suggesting that they may influence the expressive emotional system of the amygdala. On the other hand, orbitofrontal axons heavily targeted the intercalated masses, which issue inhibitory projections to the central nucleus, at least in rats and cats. The central nucleus, in turn, issues a significant inhibitory projection to hypothalamic and brainstem autonomic structures. This evidence suggests that orbitofrontal areas exercise control on the internal processing of the amygdala. In addition, the results provided direct evidence that the connections of anterior temporal visual and auditory association cortices occupy overlapping territories with the orbitofrontal cortices particularly in the posterior half of the amygdala, and specifically within the intermediate sector of the basolateral nucleus and in the magnocellular part of the basomedial nucleus (also known as accessory basal), suggesting a closely linked triadic network. This intricate network may be recruited in cognitive tasks that are inextricably linked with emotional associations.     

EEG correlates (event-related desynchronization) of emotional face elaboration: a temporal analysis

An EEG frequency band analysis was conducted, in order to explore the significance of brain oscillations (delta, theta, alpha and beta) for emotional face comprehension during different post-stimulus time intervals (50-150; 150-250; 250-350; and 350-450 ms). The study was conducted on twenty adults who looked at emotional (happy, sad, angry, fearful) or neutral faces. The results showed that motivational significance of the stimulus can modulate the power synchronization (event-related desynchronization (ERD) decrease) within the frequency band of delta and theta. We propose that delta and theta respond to variations in processing stage of emotional face: whereas, delta reflects updating of the stimulus, theta responds to the emotional significance of face. The findings revealed that emotional discrimination by theta is observable mainly within 150-250 time interval and that it is more distributed on anterior regions, whereas delta is maximally synchronized within 250-350 interval and more posteriorly distributed for all the stimulus type. Finally, a right-hemisphere dominance was found for theta during emotional face comprehension.     

Cross-correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey

Cross-correlation studies performed in cat visual cortex have shown that neurons in different cortical areas of the same hemisphere or in corresponding areas of opposite hemispheres tend to synchronize their activities. The presence of synchronization may be related to the parallel organization of the cat visual system, in which different cortical areas can be activated in parallel from the lateral geniculate nucleus. We wanted to determine whether interareal synchronization of firing can also be observed in the monkey, in which cortical areas are thought to be organized in a hierarchy spanning different levels. Cross-correlation histograms (CCHs) were calculated from pairs of single or pairs of multiunit activities simultaneously recorded in areas V1 and V2 of paralyzed and anesthetized macaque monkeys. Moving bars and flashed bars were used as stimuli. The shift predictor was calculated and subtracted from the raw CCH to reveal interactions of neuronal origin in isolation. Significant CCH peaks, indicating interactions of neuronal origin, were obtained in 11% of the dual single-unit recordings and 46% of the dual multiunit recordings with moving bars. The incidence of nonflat CCHs with flashed bars was 29 and 78%, respectively. For the pairs of recording sites where both flashed and moving stimuli were used, the incidences of significant CCHs were very similar. Three types of peaks were distinguished on the basis of their width at half-height: T (<16 ms), C (between 16 and 180 ms), and H peaks (>180 ms). T peaks were very rarely observed (<1% in single-unit recordings). H peaks were observed in 7-16% of the single-unit CCHs, and C peaks in 6-16%, depending on the stimulus used. C and H peaks were observed more often when the receptive fields were overlapping or distant by <2 degrees. To test for the presence of synchronization between neurons in areas V1 and V2, we measured the position of the CCH peak with respect to the origin of the time axis of the CCH. Only in the case of a few T peaks did we find displaced peaks, indicating a possible drive of the V2 neuron by the simultaneously recorded V1 cell. All the other peaks were either centered on the origin or overlapped the origin of time with their upper halves. Thus similarly to what has been reported for the cat, neurons belonging to different cortical areas in the monkey tend to synchronize the time of emission of their action potentials with three different levels of temporal precision. For peaks calculated from flashed stimuli, we compared the peak position with the difference between latencies of V1 and V2 neurons. There was a clear correlation for single-unit pairs in the case of C peaks. Thus the position of a C peak on the time axis appears to reflect the order of visual activation of the correlated neurons. The coupling strength for H peaks was smaller during visual drive compared with spontaneous activity. On the contrary, C peaks were seen more often and were stronger during visual stimulation than during spontaneous activity. This suggests that C-type synchronization is associated with the processing of visual information. The origin of synchronized activity in a serially organized system is discussed.     

Neuronal architecture of the human temporal cortex

Summary The cortex of the superior, middle and inferior temporal gyri of the human cerebral hemispheres was investigated using Nissl, Golgi and fibre staining techniques. Brodmann's (1909) area 41, corresponding to the primary auditory cortex in Heschl's transverse temporal gyri, consisted of typical koniocortex, and formed the middle part of the superior temporal plane (the buried lower bank of the Sylvian fissure). Anteriorly the superior temporal plane contained area 22, and posteriorly the planum temporale (part of area 42). The lateral surfaces of the superior, middle and inferior temporal gyri respectively correspond to areas 22, 21 and 20. Neurons in much of the left temporal cortex, apart from area 41, formed radial columns. This columnar organisation was most pronounced posteriorly and superiorly, so that anterior area 20 was the least columnar and area 42 the most. The right temporal cortex was markedly less columnar than the left. Golgi studies showed a variety of pyramidal and non-pyramidal neurons, with specific varieties typical of individual cortical layers.This paper represents part of a study for the degree of Ph.D. in the National University of Singapore by WYO