Recovery of normal topography in the somatosensory cortex of monkeys after nerve crush and regeneration.

After median nerve fibers to glabrous skin on the hands of monkeys were crushed and allowed to regenerate, normal topographical organization was recovered in the representation of the hand in primary somatosensory cortex. Similar recovery of normal cortical organization may underlie the sensory restoration that usually follows nerve crush injury in humans.

Thalamic connections of the dorsal and ventral premotor areas in New World owl monkeys.

Thalamic connections of two premotor cortex areas, dorsal (PMD) and ventral (PMV), were revealed in New World owl monkeys by injections of fluorescent dyes or wheat-germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). The injections were placed in the forelimb and eye-movement representations of PMD and in the forelimb representation of PMV as determined by microstimulation mapping. For comparison, injections were also placed in the forelimb representation of primary motor cortex (M1) of two owl monkeys. The results indicate that both PMD and PMV receive dense projections from the ventral lateral (VL) and ventral anterior (VA) thalamus, and sparser projections from the ventromedial (VM), mediodorsal (MD) and intralaminar (IL) nuclei. Labeled neurons in VL were concentrated in the anterior (VLa) and the medial (VLx) nuclei, with only a few labeled cells in the dorsal (VLd) and posterior (VLp) nuclei. In VA, labeled neurons were concentrated in the parvocellular division (VApc) dorsomedial to VLa. Labeled neurons in MD were concentrated in the most lateral and posterior parts of the nucleus. VApc projected more densely to PMD than PMV, especially to rostral PMD, whereas caudal PMD received stronger projections from neurons in VLx and VLa. VLd projected exclusively to PMD, and not to PMV. In addition, neurons labeled by PMD injections tended to be more dorsal in VL, IL, and MD than those labeled by PMV injections. The results indicate that both premotor areas receive indirect inputs from the cerebellum (via VLx, VLd and IL) and globus pallidus (via VLa, VApc, and MD). Comparisons of thalamic projections to premotor and M1 indicate that both regions receive strong projections from VLx and VLa, with the populations of cells projecting to M1 located more laterally in these nuclei. VApc, VLd, and MD project mainly to premotor areas, while VLp projects mainly to M1. Overall, the thalamic connectivity patterns of premotor cortex in New World owl monkeys are similar to those reported for Old World monkeys.

Ipsilateral cortical connections of dorsal and ventral premotor areas in New World owl monkeys.

In order to compare connections of premotor cortical areas of New World monkeys with those of Old World macaque monkeys and prosimian galagos, we placed injections of fluorescent tracers and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) in dorsal (PMD) and ventral (PMV) premotor areas of owl monkeys. Motor areas and injection sites were defined by patterns of movements electrically evoked from the cortex with microelectrodes. Labeled neurons and axon terminals were located in brain sections cut either in the coronal plane or parallel to the surface of flattened cortex, and they related to architectonically and electrophysiologically defined cortical areas. Both the PMV and PMD had connections with the primary motor cortex (M1), the supplementary motor area (SMA), cingulate motor areas, somatosensory areas S2 and PV, and the posterior parietal cortex. Only the PMV had connections with somatosensory areas 3a, 1, 2, PR, and PV. The PMD received inputs from more caudal portions of the cortex of the lateral sulcus and more medial portions of the posterior parietal cortex than the PMV. The PMD and PMV were only weakly interconnected. New World owl monkeys, Old World macaque monkeys, and galagos share a number of PMV and PMD connections, suggesting preservation of a common sensorimotor network from early primates. Comparisons of PMD and PMV connectivity with the cortex of the lateral sulcus and posterior parietal cortex of owl monkeys, galagos, and macaques help identify areas that could be homologous.

Cortical connections of the dorsomedial visual area in new world owl monkeys (Aotus trivirgatus) and squirrel monkeys (Saimiri sciureus).

The dorsomedial visual area (DM) is an extrastriate area that was originally described in owl monkeys as a complete representation of the visual hemifield in a heavily myelinated wedge of cortex just rostral to dorsomedial visual area V2. More recently, connections of DM in owl monkeys have been described (Krubitzer and Kaas [1993] J. Comp. Neurol 334:497-528). As part of an effort to determine whether DM exists in other primates, we compared the architecture, connections, and visual topography of DM in owl monkeys and the presumptive DM in squirrel monkeys. In both species of New World monkeys, the DM region was more heavily myelinated than adjacent cortex, and this region was connected with the first and second visual areas, the middle temporal area (MT), the medial area, the ventral posterior parietal area, the dorsointermediate area, the dorsolateral area, the ventral posterior and ventral anterior areas, the medial superior temporal area, the fundal area of the superior temporal sulcus, the inferior temporal cortex, and frontal cortex in or near the frontal eye field. In squirrel monkeys, both blob and interblob regions of V1 contributed equally to DM, whereas the blob regions provided most of the projections to V1 in owl monkeys. In squirrel monkeys, connections were also found with cortex on the ventral surface in the ventral occipital temporal sulcus. In owl monkeys and squirrel monkeys, connections were with both the upper and lower visual field representations in V1, V2, and MT, demonstrating that DM contains a complete representation of the visual field. These similarities in architecture, connections, and retinotopy argue that DM is a visual area of both owl and squirrel monkeys.

Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey.

Recent experiments in the cat have demonstrated that several response parameters, including frequency tuning, intensity tuning, and FM selectivity, are spatially segregated across the isofrequency axis. To investigate whether a similar functional organization exists in the primate, we have studied the spatial distribution of pure-tone receptive field parameters across the primary auditory cortex (AI) in six owl monkeys (Aotus trivirgatus). The distributions of binaural interaction types and onset latency were also examined. Consistent with previous studies, the primary auditory cortex contained a clear cochleotopic organization. We demonstrate here that several other properties of the responses to tonal stimuli also showed nonrandom spatial distributions that were largely independent from each other. In particular, the sharpness of frequency tuning to pure tones, intensity tuning and sensitivity, response latency, and binaural interaction types all showed spatial variations that were independent from the representation of characteristic frequency and from each other. Statistical analysis confirmed that these organizations did not reflect random distributions. The overall organizational pattern of overlaying but independent functional maps that emerged was quite similar to that seen in AI of cats and, in general, appears to reflect a fundamental organization principle of primary sensory cortical fields.

Movement representation in the dorsal and ventral premotor areas of owl monkeys: a microstimulation study.

We used intracortical microstimulation to investigate the lateral premotor cortex and neighboring areas in 14 hemispheres of owl monkeys, focusing on the somatotopic distribution of evoked movements, thresholds for forelimb movements, and the relative representation of proximal and distal forelimb movements. We elicited movements from the dorsal and ventral premotor areas (PMD, PMV), the caudal and rostral divisions of primary motor cortex (M1c, M1r), the frontal eye field (FEF), the dorsal oculomotor area (OMD; area 8b), the supplementary motor area (SMA), and somatosensory cortex (areas 3a and 3b). Area PMD was composed of architectonically distinguishable caudal and rostral subdivisions (PMDc, PMDr). Stimulation of PMD elicited movements of the hindlimb, forelimb, neck and upper trunk, face, and eyes. Hindlimb and forelimb movements were represented in the caudalmost part of PMDc. Face, neck, and eye movements were represented in the lateral and rostral parts of PMDc and in PMDr. Stimulation of PMV elicited forelimb and orofacial movements, but not hindlimb movements. Both proximal and distal forelimb movements were elicited from PMDc and PMV, although PMD stimulation elicited mainly shoulder and elbow movements, while PMV stimulation evoked primarily wrist and digit movements. Distal movements were evoked more frequently from PMV than from M1r or M1c. Across cases, the median forelimb thresholds for PMDc and PMV were 60 and 36 microA, respectively, values that differ significantly from each other and from the value of 11 microA obtained for M1r. Our observations indicate that premotor cortex is much more responsive to electrical stimulation than commonly thought, and contains a large territory from which eye movements can be elicited. These results suggest that in humans, much of the electrically excitable cortex located on the precentral gyrus, including cortex sometimes considered part of the frontal eye field, is probably homologous to the premotor cortex of nonhuman primates.

Distribution of M retinal ganglion cells in diurnal and nocturnal New World monkeys.

The topography of M ganglion cell distribution was studied in the retinae of two New World monkey species, the diurnal capuchin monkey Cebus apella and the nocturnal owl monkey Aotus azarae. Retinal whole mounts were stained by the neurofibrillar method of Gros-Schultze. As occurs with other diurnal primates, the Cebus M-ganglion cell density peaks in the foveal slope and declines towards the periphery. In the Aotus retina, the M ganglion cell density peaks in the area centralis and declines toward the periphery. In both species the cell density in the temporal, dorsal, and ventral meridians are similar for equivalent eccentricities. The cell density in the nasal meridian is higher than in the other meridians. The naso-temporal density ratio ranges between 1.2 and 4.3 in the Cebus and 1.6 and 2.2 in the Aotus. The total number of M-ganglion cells was 140,300 and 74,000 in the Cebus and Aotus retinae, respectively, corresponding to about 10% and 15.4% of the total retinal ganglion cell population in these species. The results indicate that M ganglion cells are similarly organized in both diurnal and nocturnal simians, but may be proportionally more important for the nocturnal species.

Synaptic and neurochemical characterization of parallel pathways to the cytochrome oxidase blobs of primate visual cortex.

The primary visual cortex (V1) of primates is unique in that it is both the recipient of visual signals, arriving via parallel pathways (magnocellular [M], parvocellular [P], and koniocellular [K]) from the thalamus, and the source of several output streams to higher order visual areas. Within this scheme, output compartments of V1, such as the cytochrome oxidase (CO) rich blobs in cortical layer III, synthesize new output pathways appropriate for the next steps in visual analysis. Our chief aim in this study was to examine and compare the synaptic arrangements and neurochemistry of elements involving direct lateral geniculate nucleus (LGN) input from the K pathway with those involving indirect LGN input from the M and P pathways arriving from cortical layer IV. Geniculocortical K axons were labeled via iontophoretic injections of wheat germ agglutinin-horseradish peroxidase into the LGN and intracortical layer IV axons (indirect P and M pathways to the CO-blobs) were labeled by iontophoretic injections of Phaseolus vulgaris leucoagglutinin into layer IV. The neurochemical content of both pre- and postsynaptic profiles was identified by postembedding immunocytochemistry for gamma-amino butyric acid (GABA) and glutamate. Sizes of pre- and postsynaptic elements were quantified by using an image analysis system, BioQuant IV. Our chief finding is that K LGN axons and layer IV axons (indirect input from M and P pathways) exhibit different synaptic relationships to CO blob cells. Specifically, our results show that within the CO blobs: 1) all K cell axons contain glutamate, and the vast majority of layer IV axons contain glutamate with only 5% containing GABA; 2) K axons terminate mainly on dendritic spines of glutamatergic cells, while layer IV axons terminate mainly on dendritic shafts of glutamatergic cells; 3) K axons have larger boutons and contact larger postsynaptic dendrites, which suggests that they synapse closer to the cell body within the CO blobs than do layer IV axons. Taken together, these results suggest that each input pathway to the CO blobs uses a different strategy to contribute to the processing of visual information within these compartments.

The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys.

Corpus callosum connections of parietal and motor cortex were studied in New World owl monkeys (Aotus trivirgatus) and Old World macaque monkeys (Macaca fascicularis) after multiple injections of 3H-proline and horseradish peroxidase, HRP, into one cerebral hemisphere, and extensive microelectrode mapping of architectonic Areas 3b, 1, and 2 of the other hemisphere. Results were obtained both from parasagittal brain sections cut orthogonal to the brain surface and from sections from flattened brains cut parallel to the brain surface. Cortical fields varied in density of callosal connections, and the density of connections varied according to body part within sensory representations. Thus, Area 3b had few, Area 1 had more, and Area 2 had relatively dense callosal connections. Within each of these fields, connections were much less dense for the representations of the glabrous hand and foot and much more dense for the representations of the face and trunk. For the representation of the hand, retrogradely labeled cells were extremely sparse in Area 3b, moderately sparse in Area 1, and moderate in Area 2. There were less dense callosal connections in the hand representations of Areas 3b, 1, and 2 in macaque as compared to owl monkeys. Label in posterior parietal cortex was uneven with zones of extremely dense connections. A large region of very dense callosal connections was noted in motor cortex just medial to the probable location of the hand representation. In all regions, callosally projecting cells appeared to be more broadly distributed than callosal terminations. In no region was the discontinuous arrangement of callosal connections obviously organized into an extensive pattern of mediolateral or rostrocaudal bands or strips.

Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections.

Physiological (intracortical microstimulation) and anatomical (transport of horseradish peroxidase conjugated to wheat germ agglutinin as shown by tetramethyl benzidine) approaches were combined in the same animals to reveal the locations, extents, and cortical connections of the frontal eye fields (FEF) in squirrel, owl, and macaque monkeys. In some of the same owl and macaque monkeys, intracortical microstimulation was also used to evoke eye movements from dorsomedial frontal cortex (the supplementary motor area). In addition, in all of the owl and squirrel monkeys, intracortical microstimulation was also used to evoke body movements from the premotor and motor cortex situated between the central dimple and the FEF. These microstimulation data were directly compared to the distribution of anterogradely and retrogradely transported label resulting from injections of tracer into the FEF in each monkey. Since the injection sites were limited to the physiologically defined FEF, the demonstrated connections were solely those of the FEF. To aid in the interpretation of areal patterns of connections, the relatively smooth cortex of owl and squirrel monkeys was unfolded, flattened, and cut parallel to the flattened surface. Cortex of macaque monkeys, which has numerous deep sulci, was cut coronally. Reciprocal connections with the ipsilateral frontal lobe were similar in all three species: dorsomedial cortex (supplementary motor area), cortex just rostral (periprincipal prefrontal cortex) to the FEF, and cortex just caudal (premotor cortex) to the FEF. In squirrel and owl monkeys, extensive reciprocal connections were made with cortex throughout the caudal half of the lateral fissure and, to a much lesser extent, cortex around the superior temporal sulcus. In macaque monkeys, only sparse connections were present with cortex of the lateral fissure, but extensive and dense connections were made with cortex throughout the caudal one-third to one-half of the superior temporal sulcus. In addition, very dense reciprocal connections were made with the cortex of the lateral, or inferior, bank of the intraparietal sulcus. Contralateral reciprocal connections in all three species were virtually limited to regions that correspond in location to the FEF and the supplementary motor area. The results of this study reveal connections between the physiologically defined frontal eye field and cortical regions known to participate in higher order visual processing, short-term memory, multimodal, visuomotor, and skeletomotor functions.(ABSTRACT TRUNCATED AT 400 WORDS)

Pulvinar and other subcortical connections of dorsolateral visual cortex in monkeys.

The present study used injections of neuroanatomical tracers to determine the subcortical connections of the caudal and rostral subdivisions of the dorsolateral area (DL) and the middle temporal crescent area (MT(C)) in owl monkeys (Aotus trivirgatus), squirrel monkeys (Saimiri sciureus), and macaque monkeys (Macaca fascicularis and M. radiata). Emphasis was on connections with the pulvinar. Patterns of corticopulvinar connections were related to subdivisions of the inferior pulvinar (PI) defined by histochemical or immunocytochemical architecture. Connections of DL/MT(C) were with the PI subdivisions, PICM, PICL, and PIp; the lateral pulvinar (PL); and, more sparsely, the lateral portion of the medial pulvinar (PM). In squirrel monkeys, there was a tendency for caudal DL to have stronger connections with PICL than PICM and for rostral DL/MT(C) to have stronger connections with PICM than PICL. In all three primates, DL/MT(C) had reciprocal connections with the pulvinar and claustrum; received afferents from the locus coeruleus, dorsal raphe, nucleus annularis, central superior nucleus, pontine reticular formation, lateral geniculate nucleus, paracentral nucleus, central medial nucleus, lateral hypothalamus, basal nucleus of the amygdala, and basal nucleus of Meynert/substantia innominata; and sent efferents to the pons, superior colliculus, reticular nucleus, caudate, and putamen. Projections from DL/MT(C) to the nucleus of the optic tract were also observed in squirrel and owl monkeys. Similarities in the subcortical connections of the dorsolateral region, especially those with the pulvinar, provide further support for the conclusion that the DL regions are homologous in the three primate groups.

Pyramidal cell heterogeneity in the visual cortex of the nocturnal New World owl monkey (Aotus trivirgatus).

Recent studies have revealed marked variation in pyramidal cell structure in the visual cortex of macaque and marmoset monkeys. In particular, there is a systematic increase in the size of, and number of spines in, the arbours of pyramidal cells with progression through occipitotemporal (OT) visual areas. In the present study we extend the basis for comparison by investigating pyramidal cell structure in OT visual areas of the nocturnal owl monkey. As in the diurnal macaque and marmoset monkeys, pyramidal cells became progressively larger and more spinous with anterior progression through OT visual areas. These data suggest that: 1. the trend for more complex pyramidal cells with anterior progression through OT visual areas is a fundamental organizational principle in primate cortex; 2. areal specialization of the pyramidal cell phenotype provides an anatomical substrate for the reconstruction of the visual scene in OT areas; 3. evolutionary specialization of different aspects of visual processing may determine the extent of interareal variation in the pyramidal cell phenotype in different species; and 4. pyramidal cell structure is not necessarily related to brain size.

The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus).

In the owl monkey, microelectrode mapping of Brodmann's area 19 indicates that this region contains part or all of at least 5 separate representations of the visual field, each of which adjoins the anterior border of V II and collectively are termed the third tier of cortical visual areas (V I is the first tier; V II is the second tier). Described in detail in this report is one of the third tier areas which is located on the dorsal surface and the adjacent medial wall of the occipital lobe and corresponds to a densely myelinated zone of cortex. In this dorsomedial area (DM), the representation of the horizontal meridian is partially split, and thus, like V II (see ref. 4) and the dorsolateral crescent5, DM is a second order transformation of the visual hemifield. In one abnormal owl monkey, a portion of the upper quadrant was represented twice in DM. This abnormal case may provide some clues as to how the normal pattern of visuotopic organization is established in the developing brain.

Use of Gabor elementary functions to probe receptive field substructure of posterior inferotemporal neurons in the owl monkey.

The large receptive fields of inferotemporal neurons in the owl monkey were studied with visual stimuli whose luminance profiles were one-dimensional Gabor functions, i.e. sinusoidal gratings within Gaussian envelopes. The members of one set of such patterns all had a full bandwidth at half-amplitude of 0.8 octaves, but different center frequencies and spatial extents. These spatially restricted stimuli were ideal for determining whether one or more than one spatial frequency band projected onto discrete subsections of the neuron's receptive field. The other set of Gabor stimuli comprised sine waves within Gaussian envelopes of constant size, but with different center frequencies and hence different bandwidths. These stimuli allowed assessment of the neuron's spatial frequency selectivity across the full breadth of its receptive field. Results suggest that only one orientation band and one spatial frequency band provide an input onto each inferotemporal neuron under our experimental conditions. The preferred spatial frequencies found (0.2-0.6 c/deg) were all in the very low spatial frequency range for this animal. Calculations show that about 3.5-7.0 full cycles of the optimal grating usually cover the full width of the receptive field, but the observed spatial frequency tuning is not nearly as sharp as that which would be predicted according to phase coherent linear summation. Moreover, at the preferred spatial frequency, the peak response to gratings in the constant aperture series was generally less than the response to the same preferred spatial frequency in the constant relative bandwidth series. These results suggest either incomplete phase coherent summation from contributing subgroups, non-linear processing, or both.

Photopigments and color vision in the nocturnal monkey, Aotus.

The owl monkey (Aotus trivirgatus) is the only nocturnal monkey. The photopigments of Aotus and the relationship between these photopigments and visual discrimination were examined through (1) an analysis of the flicker photometric electroretinogram (ERG), (2) psychophysical tests of visual sensitivity and color vision, and (3) a search for the presence of the photopigment gene necessary for the production of a short-wavelength sensitive (SWS) photopigment. Both electrophysiological and behavioral measurements indicate that in addition to a rod photopigment the retina of this primate contains only one other photopigment type--a cone pigment having a spectral peak ca 543 nm. Earlier results that suggested these monkeys can make crude color discriminations are interpreted as probably resulting from the joint exploitation of signals from rods and cones. Although Aotus has no functional SWS photopigment, hybridization analysis shows that Aotus has a pigment gene that is highly homologous to the human SWS photopigment gene.

Temporalis function in anthropoids and strepsirrhines: an EMG study.

The major purpose of this study is to analyze anterior and posterior temporalis muscle force recruitment and firing patterns in various anthropoid and strepsirrhine primates. There are two specific goals for this project. First, we test the hypothesis that in addition to transversely directed muscle force, the evolution of symphyseal fusion in primates may also be linked to vertically directed balancing-side muscle force during chewing (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). Second, we test the hypothesis of whether strepsirrhines retain the hypothesized primitive mammalian condition for the firing of the anterior temporalis, whereas anthropoids have the derived condition (Weijs [1994] Biomechanics of Feeding in Vertebrates; Berlin: Springer-Verlag, p. 282-320). Electromyographic (EMG) activities of the left and right anterior and posterior temporalis muscles were recorded and analyzed in baboons, macaques, owl monkeys, thick-tailed galagos, and ring-tailed lemurs. In addition, as we used the working-side superficial masseter as a reference muscle, we also recorded and analyzed EMG activity of the left and right superficial masseter in these primates. The data for the anterior temporalis provided no support for the hypothesis that symphyseal fusion in primates is linked to vertically directed jaw muscle forces during mastication. Thus, symphyseal fusion in primates is most likely mainly linked to the timing and recruitment of transversely directed forces from the balancing-side deep masseter (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). In addition, our data demonstrate that the firing patterns for the working- and balancing-side anterior temporalis muscles are near identical in both strepsirrhines and anthropoids. Their working- and balancing-side anterior temporalis muscles fire asynchronously and reach peak activity during the power stroke. Similarly, their working- and balancing-side posterior temporalis muscles also fire asynchronously and reach peak activity during the power stroke. Compared to these strepsirrhines, however, the balancing-side posterior temporalis of anthropoids appears to have a relatively delayed firing pattern. Moreover, based on their smaller W/B ratios, anthropoids demonstrate a relative increase in muscle-force recruitment of the balancing-side posterior temporalis. This in turn suggests that anthropoids may emphasize the duration and magnitude of the power stroke during mastication. This hypothesis, however, requires additional testing. Furthermore, during the latter portion of the power stroke, the late activity of the balancing-side posterior temporalis of anthropoids apparently assists the balancing-side deep masseter in driving the working-side molars through the terminal portion of occlusion.

Dark switch in the entrainment of circadian activity rhythms in night monkeys. Aotus trivirgatus humboldt.

1. The locomotor activity of the night monkey (Aotus trivirgatus) has been shown to be related to light intensity by an optimum function; here entrainment by LD cycles is examined to see whether the mechanism of synchronization of circadian periodicity in Aotus is based on this function. 2. Eleven night monkeys of various ages, previously in either a free-running phase or in LD 12:12 (10(2):10(-1) lux), were recorded in LD 12:12 with the optimal intensity (10(-1) lux) in the light part of the cycle and a suboptimal intensity (10(-3) lux) in the dark part. 3. In all cases the monkeys synchronized in such a way that their activity phase fell in the dark part of the LD cycle. 4. The implication is that Aotus is a true dark-active species, that the illumination-dependent activity maximum at 10(-1) lux does not affect the synchronization mechanism, and that the differential (direction of change) rather than proportional (absolute level) actions of light provide the decisive cue for synchronization of the circadian activity rhythm.