Area Of Macaque Monkeys Research Articles

Ultra-high field fMRI identifies an action-observation network in the common marmoset

The observation of others’ actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in social action monitoring, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New-World primates, which separated from Old-Word primates ~35 million years ago. Here we used ultra-high field fMRI at 9.4 T in awake common marmosets (Callithrix jacchus) while they watched videos depicting goal-directed (grasping food) or non-goal-directed actions. The observation of goal-directed actions activates a temporo-parieto-frontal network, including areas 6 and 45 in premotor/prefrontal cortices, areas PGa-IPa, FST and TE in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal cortex. These results show overlap with the humans and macaques’ AON, demonstrating the existence of an evolutionarily conserved network that likely predates the separation of Old and New-World primates.

Inferring decoding strategies for multiple correlated neural populations.

Studies of neuron-behaviour correlation and causal manipulation have long been used separately to understand the neural basis of perception. Yet these approaches sometimes lead to drastically conflicting conclusions about the functional role of brain areas. Theories that focus only on choice-related neuronal activity cannot reconcile those findings without additional experiments involving large-scale recordings to measure interneuronal correlations. By expanding current theories of neural coding and incorporating results from inactivation experiments, we demonstrate here that it is possible to infer decoding weights of different brain areas at a coarse scale without precise knowledge of the correlation structure. We apply this technique to neural data collected from two different cortical areas in macaque monkeys trained to perform a heading discrimination task. We identify two opposing decoding schemes, each consistent with data depending on the nature of correlated noise. Our theory makes specific testable predictions to distinguish these scenarios experimentally without requiring measurement of the underlying noise correlations.

Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey

Studies in humans and monkeys report widespread multisensory interactions at or near primary visual and auditory areas of neocortex. The range and scale of these effects has prompted increased interest in interconnectivity between the putatively "unisensory" cortices at lower hierarchical levels. Recent anatomical tract-tracing studies have revealed direct projections from auditory cortex to primary visual area (V1) and secondary visual area (V2) that could serve as a substrate for auditory influences over low-level visual processing. To better understand the significance of these connections, we looked for reciprocal projections from visual cortex to caudal auditory cortical areas in macaque monkeys. We found direct projections from area prostriata and the peripheral visual representations of area V2. Projections were more abundant after injections of temporoparietal area and caudal parabelt than after injections of caudal medial belt and the contiguous areas near the fundus of the lateral sulcus. Only one injection was confined to primary auditory cortex (area A1) and did not demonstrate visual connections. The projections from visual areas originated mainly from infragranular layers, suggestive of a "feedback"-type projection. The selective localization of these connections to peripheral visual areas and caudal auditory cortex suggests that they are involved in spatial localization.

Heterogeneity of the developmental patterns of neurotrophin protein levels among neocortical areas of macaque monkeys

Based on morphological and physiological characteristics, the mammalian neocortex is divided into various neocortical areas and its diversity is prominent in the primates including humans. These neocortical areas are constructed during development, but the details of the developmental events remain unclear, especially at the molecular level. We measured the mRNA and protein levels of neurotrophins in various neocortical areas of developing rhesus monkeys. The expression patterns of both the neurotrophin-3 (NT-3) mRNA and the protein showed area differences. In the sensory and motor areas, NT-3 mRNA and protein levels had started to decline by a week after birth. In contrast, the levels declined after the third postnatal week in the association neocortical areas. The level of brain-derived neurotrophic factor (BDNF) protein changed in an area-dependent manner during development, but that of mRNA did not. The decline of the BDNF protein level started earlier in the sensory and motor neocortical areas than in the association neocortical areas, suggesting that sensory and motor neocortical areas develop earlier than the association areas in terms of the developmental changes in neurotrophins.

Organization of prefrontal outflow toward frontal motor-related areas in macaque monkeys.

Linkage between the prefrontal cortex and the primary motor cortex is mediated by nonprimary motor-related areas of the frontal lobe. In an attempt to analyse the organization of the prefrontal outflow from area 46 toward the frontal motor-related areas, we investigated the pattern of projections involving the higher-order motor-related areas, such as the presupplementary motor area (pre-SMA) and the rostral cingulate motor area (CMAr). Tracer injections were made into these motor-related areas (their forelimb representation) on the medial wall that had been identified electrophysiologically. The following data were obtained from a series of tract-tracing experiments in Japanese monkeys. (i) Only a few neurons in area 46 were retrogradely labelled from the pre-SMA and CMAr; (ii) terminal labelling from area 46 occurred sparsely in the pre-SMA and CMAr; (iii) a dual labelling technique revealed that the sites of overlap of anterograde labelling from area 46 and retrograde labelling from the pre-SMA and CMAr were evident in the rostral parts of the dorsal and ventral premotor cortices (PMdr and PMvr); (iv) and tracer injections into the PMdr produced neuronal cell labelling in area 46 and terminal labelling in the pre-SMA and CMAr. The present results indicate that a large portion of the prefrontal signals from area 46 is not directly conveyed to the pre-SMA and CMAr, but rather indirectly by way of the PMdr and PMvr. This suggests that area 46 exerts its major influence on the cortical motor system via these premotor areas.

Ascending inputs to the pre-supplementary motor area in the macaque monkey: cerebello- and pallido-thalamocortical projections

The goal of the present study was to determine the ascending sources to the pre-supplementary motor area (pre-SMA) in macaque monkeys using multiple labeling techniques. We labeled the pallidothalamic projections using biotinylated dextran amine (BDA) and the cerebellothalamic projections using wheatgerm agglutinin conjugated to horseradish peroxidase. The pre-SMA thalamocortical projections neurons were also labeled using cholera toxin subunit b following identification of the pre-SMA by location, and by movements evoked by intracortical microstimulation. The extent of pre-SMA was later confirmed by identifying characteristics from Nissl cytoarchitecture and SMI-32 immunoreactivity. Thalamic nuclear boundaries were based on Nissl cytoarchitecture, acetylcholinesterase chemoarchitecture and Cat-301 immunoreactivity. Cerebellothalamic afferents were distributed predominantly to ventral lateral posterior nucleus (VLp), including medial and dorsal VLp, while the pallidothalamic afferents projected more rostrally to ventral lateral anterior nucleus (VLa) and ventral anterior nucleus (VA). The pre-SMA thalamocortical projection neurons were primarily found in VA and medial VLp. However, scattered cells were also found in VLa, dorsal VLp, central lateral nucleus (CL) and mediodorsal nucleus (MD). Scattered pre-SMA projecting cells overlapped foci of cerebellar label in medial VLp. Additionally, limited overlap of pre-SMA cells and pallidothalamic labeling was found in caudal VA. These findings suggest that the pre-SMA is uniquely positioned to integrate ascending basal ganglia and cerebellar information after a relay from VA and medial VLp. These anatomical findings are consistent with the recent hypothesis that the pre-SMA acts as the coordinator of visual and motor loops in motor learning [J. Cogn. Neurosci. 13 (2001) 626].

Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys.

To gain insight into how cortical fields process somatic inputs and ultimately contribute to complex abilities such as tactile object perception, we examined the pattern of connections of two areas in the lateral sulcus of macaque monkeys: the second somatosensory area (S2), and the parietal ventral area (PV). Neuroanatomical tracers were injected into electrophysiologically and/or architectonically defined locations, and labeled cell bodies were identified in cortex ipsilateral and contralateral to the injection site. Transported tracer was related to architectonically defined boundaries so that the full complement of connections of S2 and PV could be appreciated. Our results indicate that S2 is densely interconnected with the primary somatosensory area (3b), PV, and area 7b of the ipsilateral hemisphere, and with S2, 7b, and 3b in the opposite hemisphere. PV is interconnected with areas 3b and 7b, with the parietal rostroventral area, premotor cortex, posterior parietal cortex, and with the medial auditory belt areas. Contralateral connections were restricted to PV in the opposite hemisphere. These data indicate that S2 and PV have unique and overlapping patterns of connections, and that they comprise part of a network that processes both cutaneous and proprioceptive inputs necessary for tactile discrimination and recognition. Although more data are needed, these patterns of interconnections of cortical fields and thalamic nuclei suggest that the somatosensory system may not be segregated into two separate streams of information processing, as has been hypothesized for the visual system. Rather, some fields may be involved in a variety of functions that require motor and sensory integration.

A spatially organized representation of colour in macaque cortical area V2.

Neurons responding selectively to different colours have been found in various cortical areas in macaque monkeys; however, little is known about whether and how the representation of colour is spatially organized in any cortical area. Cortical area V2 contains modules that respond preferentially to chromatic modulation, which are located in thin cytochrome oxidase stripes. Here we show that within and beyond these modules, gratings of different colours produce activations that peak at different locations. Optical recording of intrinsic signals revealed that the peak regions of the responses to different colours were spatially organized in the same order as colour stimuli are arranged in the DIN (German standard colour chart) colour system. Nearby regions represented colours of a similar hue. We found that the set of colour-specific regions formed 0.07-0.32-mm-wide and approximately 1.3-mm long bands that varied in shape from linear to nearly circular. Our finding suggests that thin stripes in V2 contain functional maps where the colour of a stimulus is represented by the location of its response activation peak.

Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans.

The internal organization of a higher level visual area in the human parietal cortex was mapped. Functional magnetic resonance images were acquired while the polar angle of a peripheral target for a delayed saccade was gradually changed. A region in the superior parietal cortex showed robust retinotopic mapping of the remembered target angle. The map reversed when the direction of rotation of the remembered targets was reversed and persisted unchanged when study participants detected rare target reappearances while maintaining fixation, or when the eccentricity of successive remembered targets was unpredictable. This region may correspond to the lateral intraparietal area in macaque monkeys.

Investigation of cooperative cortical dynamics by multivariate autoregressive modeling of event-related local field potentials

To explore the operation of large-scale networks in the cerebral cortex, we sought to measure the functional interdependence of event-related local field potentials (LFPs) from different cortical areas in macaque monkeys performing a visuomotor pattern discrimination task. To track the transformation of functional interdependence accompanying rapid changes in cognitive state, we developed a method for spectral coherence analysis using multivariate autoregressive (MVAR) models of short-windowed LFP time series. MVAR modeling overcomes problems associated with direct coherence analysis of short-windowed data. Coherence and phase are shown to vary during task processing with spatial location, processing stage, and stimulus and response conditions.

Dual morphology and topography of the corticothalamic terminals originating from the primary, supplementary motor, and dorsal premotor cortical areas in macaque monkeys.

In the motor, somatosensory, and auditory systems of rodents and cats, the corticothalamic connection is composed of a main projection formed by small endings and a minor projection terminating with giant endings. To establish whether the corticothalamic projection originating from motor cortical areas in primates exhibits the same duality, the anterograde tracer biotinylated dextran amine was injected in eight macaque monkeys in the primary motor (M1; n = 3), the supplementary motor (SMA; n = 3) and the dorsal premotor (PMd; n = 2) cortical areas to label corticothalamic axons. The corticothalamic projection originating from these three motor cortical areas was characterized by the presence of axon terminals constituting the same two types of endings, observed both as boutons en passant and terminaux. The population of small endings exhibited a mean cross-sectional maximum diameter of 0.95 microm (S.D. = 0.23), a range of diameters not overlapping that of giant endings (mean diameter = 3.46 microm, S.D. = 0.74 microm). Topographically, the giant endings originating from M1 were located in the same thalamic nucleus (ventroposterolateral nucleus, oral part) in which the small endings were found. In contrast, the giant endings originating from SMA and PMd were located in a thalamic nucleus (mediodorsal nucleus) distinct from the main termination zone formed by small endings. Along the rostrocaudal axis, the giant endings were distributed in a restricted zone, irrespective of the origin of the projection (M1, SMA, PMd). The dual morphology of corticothalamic endings, previously found in rodents and cats, is present in the motor system of subhuman primates for both primary and nonprimary motor cortical areas.

Modular Organization of Occipito-Temporal Pathways: Cortical Connections between Visual Area 4 and Visual Area 2 and Posterior Inferotemporal Ventral Area in Macaque Monkeys

The modular organization of cortical pathways linking visual area 4 (V4) with occipital visual area 2 (V2) and inferotemporal posterior inferotemporal ventral area (PITv) was investigated through an analysis of the patterns of retrogradely labeled cell bodies after injections of tracers into V4 and PITv. Although cytochrome oxidase or other stains have failed to yield reliable independent anatomical markers for cortical modules beyond V1 and V2, V4 and PITv seem to have modular compartments with specific patterns of cortico-cortical connectivity. Tracer injections of V4 labeled cells in V2 (1) thin stripes exclusively, (2) interstripes exclusively, or (3) specific combinations of interstripe and thin stripe subcompartments. These labeling patterns suggest (1) that there is a complicated organization of inputs to V4, (2) that projections from V2 to V4 display a submodular selectivity, and (3) that projections from V2 to V4 display some degree of cross-stream convergence. Consistent with this framework, extensive regions of PITv provide feedback projections to interstripe-recipient portions of V4, whereas more restricted portions of PITv provide feedback to thin stripe-recipient portions of V4. Similarly, the feedforward projection from V4 to PITv often arose from multiple cell clusters across a wide expanse of V4. When distinguishable fluorescent tracers were injected into two PITv sites separated by 3-5 mm, a variety of projection patterns was observed in V4. In most cases, labeled cells were found in multiple, interdigitating, nonoverlapping clusters of 1-3 mm width, whereas in other cases the two labeled fields were highly intermixed. These results suggest that V4 and PITv contain functional modules that can be characterized by the specific patterns of segregated and convergent projections they receive from lower cortical areas. These specific patterns of intercortical input, in conjunction with intrinsic cortical circuitry, may endow extrastriate cortical neurons with new and more complex receptive field properties.

Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys

Cortical connections between various body representations in areas 3b and 1 and lateral parietal cortex were examined in 18 macaque monkeys. We injected tracers (Fast Blue, Diamidino Yellow, Horseradish Peroxidase, and Rhodamine Dextran), alone or in combination, into closely related cutaneous responsive sites, e.g., adjacent digits. Separated patches of labeling were found across the parietal operculum and insula for all injected locations. On the basis of cytoarchitectural criteria, the labeled regions include the second somatosensory area (SII), retroinsular area (Ri) and granular insula (Ig). Assuming the connections are homotopical from physiologically identified body representations in primary somatosensory cortex, the labeling patterns in SII include complete anterior and posterior body maps. The orientation of the body is erect in the posterior and supine in the anterior SII region. Area 3b has greater density of connections with anterior SII. The maps are mirror images aligned along the distal extremities. The anterior-posterior (A-P) length of the "SII region" exceeds 7 mm; it extends in the coronal plane from the fundus of the lateral sulcus to surface cortex near the anterior tip of the intraparietal sulcus. Two additional topographically organized maps are likely in Ri. These are "worm-like" body maps oriented along the A-P axis and joined at the head representation. Connections with the center of Ig are not somatotopically organized. The diversity of somatosensory areas in lateral parietal cortex revealed by the labeled connections was discussed in reference to prior mapping of SII in monkeys and was compared to reports of multiple areas in this region of cortex in other species.

Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys.

The goal of the present neuroanatomical study in macaque monkeys was twofold: (1) to clarify whether the hand representation of the primary motor cortex (M1) has a transcallosal projection to M1 of the opposite hemisphere; (2) to compare the topography and density of transcallosal connections for the hand representations of M1 and the supplementary motor area (SMA). The hand areas of M1 and the SMA were identified by intracortical microstimulation and then injected either with retrograde tracer substances in order to label the neurons of origin in the contralateral motor cortical areas (four monkeys) or, with an anterograde tracer, to establish the regional distribution and density of terminal fields in the opposite motor cortical areas (two monkeys). The main results were: (1) The hand representation of M1 exhibited a modest homotopic callosal projection, as judged by the small number of labeled neurons within the region corresponding to the contralateral injection. A modest heterotopic callosal projection originated from the opposite supplementary, premotor, and cingulate motor areas. (2) In contrast, the SMA hand representation showed a dense callosal projection to the opposite SMA. The SMA was found to receive also dense heterotopic callosal projections from the contralateral rostral and caudal cingulate motor areas, moderate projections from the lateral premotor cortex, and sparse projections from M1. (3) After injection of an anterograde tracer (biotinylated dextran amine) in the hand representation of M1, only a few small patches of axonal label were found in the corresponding region of M1, as well as in the lateral premotor cortex; virtually no label was found in the SMA or in cingulate motor areas. Injections of the same anterograde tracer in the hand representation of the SMA, however, resulted in dense and widely distributed axonal terminal fields in the opposite SMA, premotor cortex, and cingulate motor areas, while labeled terminals were clearly less dense in M1. It is concluded that the hand representations of the SMA and M1 strongly differ with respect to the strength and distribution of callosal connectivity with the former having more powerful and widespread callosal connections with a number of motor fields of the opposite cortex than the latter. These anatomical results support the proposition of the SMA being a bilaterally organized system, possibly contributing to bimanual coordination.

The hippocampal CA1 connections with the inferotemporal and parahippocampal cortical areas in macaque monkeys

The hippocampal CA1 connections with the inferotemporal and parahippocampal cortical areas in macaque monkeys

Second somatosensory cortical area in macaque monkeys. I. Neuronal responses to controlled, punctate indentations of glabrous skin on the hand

Responses of 492 single neurons from the second somatosensory cortical area of macaque monkeys were studied using computer controlled ramp indentations. Results were obtained using chronic recording techniques from lightly tranquilized or awake animals. Amongst those cells that were activated by punctate tactile stimuli, various subclasses of responses were identified that included neurons with phasic and sustained adaptation characteristics. In addition, several cells showed unusual firing patterns, such as delayed responses and reverberating afterdischarges. Latency measurements from 90 cells showed a modal latency to ramp stimuli of 34 ms and a second group of cells whose latency exceeded 75 ms. Measurements of response functions to different velocities of indentation revealed that some cells maintained relatively shallow ascending functions but that most cells were insensitive to the velocity variable. The response characteristics of these neurons in primates are discussed in reference to the hypothesis that in the somatosensory cortex, SII occupies a higher order, serially dependent region in a hierarchy from SI to other parts of the brain.

Differential contributions to coding of cutaneous vibratory information by cortical somatosensory areas I and II.

Differential contributions to coding of cutaneous vibratory information by cortical somatosensory areas I and II.

Cortical projection to hand-arm motor area from post-arcuate area in macaque monkeys: A histological study of retrograde transport of horseradish peroxidase

In four macaque monkeys horseradish peroxidase (HRP) was injected into physiologically defined hand-arm motor area. Ipsilaterally, HRP labeled neurons were found in both upper and lower limbs of the posterior bank of the arcuate sulcus and in an area surrounding the arcuate spur. Contralaterally, labeled neurons were found in the same areas, though less dense in concentration. Labeled neurons were found mostly in layer III of the cortex.