Pulvinar Of Monkeys Research Articles

Neural Mechanisms of Innate Recognition of Facial Stimuli in Primates

Primates can recognize or respond to specific stimuli that are important for survival, such as faces, predators, prey animals, and foods, even if they have not experienced those stimuli previously (innate recognition). Throughout vertebrates, including primates, the extrageniculate visual system (subcortical visual pathway) comprising the retina, superior colliculus, pulvinar, and amygdala is thought to be genetically hard-wired and involved in innate recognition of these stimuli. To investigate neural mechanisms of innate recognition in primates, we analyzed single neuronal responses to facial images in the monkey pulvinar and superior colliculus. The results indicated that the pulvinar and superior collicular neurons responded preferentially to facial images in short latency and showed gamma oscillations during stimulus presentation. Furthermore, the population activity of these neurons discriminated head direction, sex, and identity of facial images. Based on these findings, we discussed neural mechanisms underlying the innate and automatic (unconscious) detection of facial stimuli in the extrageniculate visual system.

Population Coding of Facial Information in the Monkey Superior Colliculus and Pulvinar.

The superior colliculus (SC) and pulvinar are thought to function as a subcortical visual pathway that bypasses the striate cortex and detects fundamental facial information. We previously investigated neuronal responses in the SC and pulvinar of monkeys during a delayed nonmatching-to-sample task, in which the monkeys were required to discriminate among 35 facial photos of five models and other categories of visual stimuli, and reported that population coding by multiple SC and pulvinar neurons well discriminated facial photos from other categories of stimuli (Nguyen et al., 2013, 2014). However, it remains unknown whether population coding could represent multiple types of facial information including facial identity, gender, facial orientation, and gaze direction. In the present study, to investigate population coding of multiple types of facial information by the SC and pulvinar neurons, we reanalyzed the same neuronal responses in the SC and pulvinar; the responses of 112 neurons in the SC and 68 neurons in the pulvinar in serial 50-ms epochs after stimulus onset were reanalyzed with multidimensional scaling (MDS). The results indicated that population coding by neurons in both the SC and pulvinar classified some aspects of facial information, such as face orientation, gender, and identity, of the facial photos in the second epoch (50–100 ms after stimulus onset). The Euclidean distances between all the pairs of stimuli in the MDS spaces in the SC were significantly correlated with those in the pulvinar, which suggested that the SC and pulvinar function as a unit. However, in contrast with the known population coding of face neurons in the temporal cortex, the facial information coding in the SC and pulvinar was coarse and insufficient. In these subcortical areas, identity discrimination was face orientation-dependent and the left and right profiles were not discriminated. Furthermore, gaze direction information was not extracted in the SC and pulvinar. These results suggest that the SC and pulvinar, which comprise the subcortical visual pathway, send coarse and rapid information on faces to the cortical system in a bottom-up process.

Neuronal responses to face‐like stimuli in the monkey pulvinar

The pulvinar nuclei appear to function as the subcortical visual pathway that bypasses the striate cortex, rapidly processing coarse facial information. We investigated responses from monkey pulvinar neurons during a delayed non-matching-to-sample task, in which monkeys were required to discriminate five categories of visual stimuli [photos of faces with different gaze directions, line drawings of faces, face-like patterns (three dark blobs on a bright oval), eye-like patterns and simple geometric patterns]. Of 401 neurons recorded, 165 neurons responded differentially to the visual stimuli. These visual responses were suppressed by scrambling the images. Although these neurons exhibited a broad response latency distribution, face-like patterns elicited responses with the shortest latencies (approximately 50 ms). Multidimensional scaling analysis indicated that the pulvinar neurons could specifically encode face-like patterns during the first 50-ms period after stimulus onset and classify the stimuli into one of the five different categories during the next 50-ms period. The amount of stimulus information conveyed by the pulvinar neurons and the number of stimulus-differentiating neurons were consistently higher during the second 50-ms period than during the first 50-ms period. These results suggest that responsiveness to face-like patterns during the first 50-ms period might be attributed to ascending inputs from the superior colliculus or the retina, while responsiveness to the five different stimulus categories during the second 50-ms period might be mediated by descending inputs from cortical regions. These findings provide neurophysiological evidence for pulvinar involvement in social cognition and, specifically, rapid coarse facial information processing.

Emotion recognition following human pulvinar damage

Pulvinar activation has been observed while viewing fearful expressions, but the necessity of this activation to their recognition has not been previously assessed. We measured the processing of emotional facial expressions in a rare patient with complete unilateral loss of the pulvinar. With brief presentations, patient CJ was incapable of recognizing fearful expressions in his contralesional field. Three other patients, with damage limited to the anterior and to the lateral pulvinar, showed no deficits in recognition. In conjunction with anatomical studies of the monkey pulvinar, these results suggest that fear recognition is mediated by the human medial pulvinar. We outline the possible role of the pulvinar in fear recognition, considering both the pulvinar's direct and indirect cortical connections with the amygdala, and we suggest that the integrative role of the pulvinar may be primary. Our results suggest that the cortex in isolation from the entire pulvinar is incapable of recognizing fearful expressions.

Comparative physiological and serotoninergic properties of pulvinar neurons in the monkey, cat and ferret

The basic electrophysiological properties and responses to serotonin of thalamocortical (TC) neurons in the ferret, cat, and monkey pulvinar were compared. Morphologically, thalamocortical neurons in these three species were similar, except for the presence of beaded dendrites in many monkey neurons. In all three species, the neurons exhibited two distinct firing modes: single spike activity and low threshold Ca 2+-spike mediated bursting. However, in monkeys, the low threshold Ca 2+ spikes were followed by a prominent 50–100 ms afterhyperpolarization that could result in the generation of an additional rebound Ca 2+ spike. The application of 5-HT to thalamocortical neurons in cat and monkey pulvinar resulted in a depolarization and an increase in membrane conductance through an enhancement of the hyperpolarization-activated cation current, I h, apparently through the activation of 5-HT 7 receptors. In contrast, the application of serotonin to ferret pulvinar neurons resulted in a prominent hyperpolarization, owing to an increase in membrane potassium conductance. In monkey and ferret, application of serotonin could result in barrages of IPSPs in thalamocortical neurons. These results indicate that there are significant species-dependent differences in both the electrophysiological and pharmacological properties of pulvinar thalamocortical neurons.

Deficits in spatial coding and feature binding following damage to spatiotopic maps in the human pulvinar.

We report a patient with unilateral damage to the rostral part of the pulvinar who was impaired in localizing stimuli in the inferior visual field contralateral to the lesion and who made errors in the binding of shape and color in that quadrant. The findings demonstrate the importance of the pulvinar in spatial coding and provide support for the function of the thalamus in binding of features. They also provide evidence for a homology between the visual field maps of the inferior and lateral subdivisions of the pulvinar in monkeys and in humans, such that the inferior visual field is represented in the rostral part of the nucleus.

Thalamic connections of the dorsomedial visual area in primates

The dorsomedial visual area (DM) of owl monkeys is a cortical area that has been described recently in a range of primate species. To study the thalamic connections of this area, injections of several distinguishable neuroanatomical tracers were placed into DM in galagos, owl monkeys, squirrel monkeys, and macaque monkeys. The distribution of label was remarkably consistent across these diverse primate species. Labeled connections were densest within the pulvinar complex. Both the lateral and inferior divisions of the pulvinar, but not the medial division, had connections with DM. Within the inferior pulvinar of monkeys, central lateral and central medial nuclei had dense connections, and the medial and posterior nuclei had sparse connections with DM. Sparser connections were revealed in the lateral geniculate nucleus and the nucleus limitans. Anterograde label was also found in the superior colliculus. The consistencies in the pattern of subcortical projections across prosimian primates, New World monkeys, and Old World monkeys support the concept that DM is a visual area common to all primates. In addition, these results provide further evidence for proposed subdivisions of the inferior pulvinar.

Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr.

The organization of the inferior pulvinar complex (PI) in squirrel monkeys was studied with histochemical localization of the calcium binding proteins calbindin-D28k and parvalbumin, and of cytochrome oxidase. With each of these markers, the inferior pulvinar complex can be subdivided into four distinct regions. Calbindin-D28k immunoreactivity is densely distributed in cells and neuropil within PI, except for a distinct centromedially located gap. This calbindin-poor zone, termed the medial division of the inferior pulvinar (PIM), corresponds precisely to a region that contains elevated cytochrome oxidase activity and parvalbumin immunostaining. The PIM extends slightly above and behind the classically defined limit of the inferior pulvinar, the corticotectal tract. Regions of inferior pulvinar with intense immunostaining for calbindin-D28k were the posterior division of the inferior pulvinar (PIP, medial to PIM) and the central division (PIC, lateral to PIM). A newly recognized lateral region, PIL, adjoins the lateral geniculate nucleus and stains more lightly for calbindin and parvalbumin immunoreactivity and for cytochrome oxidase. Staining patterns for calbindin, parvalbumin, and cytochrome oxidase in the pulvinar of rhesus monkeys closely resemble those shown in squirrel monkey inferior pulvinar, suggesting that a common organization exists in all primates. In order to examine cortical connection patterns of the histochemically defined compartments in the inferior pulvinar, injections of up to five neuroanatomical tracers (wheat germ agglutinin conjugated to horseradish peroxidase and fluorescent retrograde tracers) were placed in the same cerebral hemisphere. Single injection sites were in the middle temporal area (MT), and several separate injections were placed in a strip corresponding to the rostral subdivision of the dorsolateral area (DLr). Injections that involved only DLr and not MT labeled principally the PIC, and more sparsely PIP and PIL. DLr connections occupied a "shell" region dorsal to PIM that extended from PIC into the lateral and medial divisions of the pulvinar, PL and PM. Injection sites that included MT or were largely restricted to MT produced dense label in PIM and moderate label in PIC and PIL. The retinotopic organization within the inferior pulvinar was inferred from patterns of connections. Connections with cortex related most closely to central vision were found posteriorly in PIM and in adjacent portions of PIC as it wraps around the caudal pole of PIM. Cortex related to more peripheral locations in the lower visual field connected with more rostral PIM and PIC. Patterns of label within the portions of PL and PM that were immediately adjacent to PIM roughly paralleled those in PIM and PIC.(ABSTRACT TRUNCATED AT 400 WORDS)

Saccadic eye movements following kainic acid lesions of the pulvinar in monkeys

Behavioral and anatomical experiments have suggested that the pulvinar might play a role in the generation of saccadic eye movements to visual targets. To test this idea, we trained monkeys to make visually-guided saccades by requiring them to detect the dimming of a small target. We used three different saccade paradigms. On single-step trials, saccades were made from a central fixation point (FP) to a target at 12, 24 or 36 degrees to the left or right. On overlap trials, the FP remained lit during presentation of a target at 12 or 24 degrees. On double-step trials, the target stepped first to 24 degrees, and then back to 12 degrees on the same side. Animals were trained to criterion, received kainic acid lesions of the pulvinar, and were retested on all three tasks. The lesions were very large, destroying almost all of the visually responsive pulvinar. They also encroached on the lateral geniculate nucleus, thereby producing small foveal scotomas, and this resulted in some behavioral changes, including difficulty in maintaining fixation on the target and in detecting its dimming. Results on the saccade tests suggest that the pulvinar is not crucial for initiation of saccadic eye movements. Saccade latency and amplitude were unimpaired on both single-step and overlap trials. Saccadic performance was also normal on double-step trials. In a second experiment, we measured the average length of fixations during spontaneous viewing of a complex visual scene. Fixation lengths did not differ from those of unoperated control monkeys. We suggest that the neglect, increased saccadic latencies, and prolonged fixations attributed to pulvinar damage in previous studies were probably the result instead of inadvertent damage to tectal afferents. The present results, together with single unit data, point to a role for the pulvinar not in the generation of saccades, but rather in the integration of saccadic eye movements with visual processing.

The prenatal development of the pulvinar in the monkey: 3H-thymidine autoradiographic and morphometric analyses.

The genesis and development of the pulvinar in monkey (Macaca mulatta) was studied by means of tritiated thymidine (3H-TdR) autoradiography and by examination and morphometric analysis of Nissl stained histological sections. The time of origin was determined by analysis of labeled cells in the pulvinar of monkeys that had been exposed to 3H-TdR at various embryonic (E) days and sacrificed 2–3 months after birth, which in this species occurs around E165. Heavily labeled pulvinar neurons were observed only in animals that had been exposed to 3H-TdR between E36 and E45. Onset of genesis for neurons that comprise the inferior and adjacent areas of lateral pulvinar precedes the onset in the remainder of lateral and medial pulvinar by two days. The site of origin and migratory pathways of pulvinar neurons were determined in a series of animals that had been exposed to 3H-TdR between E36 and E45 and sacrificed 1 h or 1, 3, 7, 14, and 42 days after injection. No neurons are produced within the pulvinar. Rather, they arise exclusively from the diencephalic ventricular and subventricular zones that border the third ventricle between sulcus medius and sulcus dorsalis. Postmitotic cells migrate laterally and in less than 3 days attain their position at the lateral aspect of the developing thalamus where they remain uniformly distributed during the first half of gestation. The cytoarchitectonic boundaries of the pulvinar are distinguished from adjacent thalamic nuclei by E60 whereas its own subdivisions emerge around E80. Morphometric analysis shows that the increase in the size of the pulvinar of the monkey during the last two thirds of gestation is due to cell growth, elaboration of cell processes, and arrival of various afferent inputs rather than to the influx of newly generated neurons, as in the human brain (Rakic and Sidman 1969). Instead the present data indicate that the pulvinar in monkey is generated much earlier than expected from previous studies and that unlike the human pulvinar, does not contain a subpopulation of neurons of telencephalic origin.

The morphology and distribution of striate cortex terminals in the inferior and lateral subdivisions of the Macaca monkey pulvinar.

The origin of the various types of axon terminals in Macaca pulvinar remains uncertain because of the contradictory results obtained in EM degeneration studies. We have used EM-autoradiography to determine the morphology of terminals in the inferior and lateral pulvinar which originate from neurons in visual cortex. After injections of H3 proline into area 17, both the small diameter (RS) and the large diameter (RL) terminals containing round vesicles and making asymmetric contacts are labeled in the two pulvinar subdivisions. Labeled and unlabeled terminals are intermixed within the pulvinar focus which suggests that the dendrites of the same pulvinar neuron receive overlapping inputs from several cortical areas. Because only 5% of the pulvinar terminals are RLs (Ogren and Hendrickson, '79), and this small number of RLs originates from at least two visual cortical areas plus the superior colliculus (Partlow et al., '77), superior colliculus input to inferior pulvinar is small compared to the combined RS and RL cortical input. Together the findings from this study and the preceding paper (Ogren and Henderickson, '79), show that while pulvinar is typical of other thalamic nuclei in the structure of its neurons and synapses, it differs in that the input from subcortical structures is minimal. It is suggested that inferior and lateral pulvinar function principally as integrators of visula cortical information.

A review of cat and monkey studies implicating the pulvinar in visual function

The anatomical, neurophysiological, and behavioral evidence implicating the cat's and monkey's pulvinar in visual function is reviewed. While at present it is not possible to establish homologies between regions of the posterior thalamus in these two species, in both species there is evidence for extra-geniculate pathways by which visual input could be relayed to cortex. In the monkey, it is suggested that the inferior pulvinar could be part of a subcortical system dealing with visual attentional function, while portions of the medial pulvinar could be involved in a system concerned with oculomotor integration.

Effect of pulvinar lesions on visual pattern discrimination in monkeys.

This study compares the performance (percent correct responses and reaction times) of three unoperated control monkeys with the postoperative performance of eight monkeys with pulvinar lesions, either inferior pulvinar or medial and lateral pulvinar, on a tachistoscopically presented visual pattern-discrimination task highly demanding of attention. To further emphasize and assess the attentional factor in visual pattern discrimination, all monkeys who attained criterion performance (90% correct response on three consecutive sessions of 100 trials each) were tested for the effects of visually distracting interference stimuli added to the original discriminative stimuli. In addition, retention of postoperatively learned discriminations was tested after a 6-wk interval withou training and compared with the performance of control monkeys. Four monkeys with only inferior pulvinar lesions and one monkey with inferior pulvinar plus medial and lateral pulvinar lesions were markedly impaired in the postoperative learning of a visual pattern discrimination. Three of these monkeys failed to acquire criterion perfromance in 9,000 or more training trials, while two learned to ceiterion level only after prolonged training (7,400 and 6,900 trials). In contrast, monkeys with medial and lateral pulvinar lesions showed no deficit in learning ability compared to unoperated control monkeys. Furthermore, the performance of the two monkeys with inferior pulvinar lesions, who attained the criterion level of learning only with difficulty, was further impaired by the addition of distracting interference stimuli, where the performance of monkeys with medial and lateral pulvinar lesions as well as the control monkeys was only temporarily disrupted by this procedure. None of the monkeys with pulvinar lesions, who were tested for retention of the postoperatively learned discrimination, showed appreciable deficits in comparison to control monkeys. All monkeys, including controls and those uith pulvinar lesions who were able to learn the visual pattern discrimination, showed a common pattern of reaction time (RT) change during the course of the learning; that is, RT was low during change-level performance, increased during learning, and decreased once criterion performance was achieved. Reaction times of monkeys with inferior pulvinar lesions tended to be longer than for controls or for those with medial and lateral pulvinar lesions. These results provide the first behavior evidence that the inferior pulvinar of monkeys is involved in visual pattern discrimination and add further support to the concept of a second visual system in which the inferior pulvinar plays a role. The attentional aspects of the visual pattern-discrimination task employed in this study and the additional effects obtained with distracting stimuli suggest that the impairments arising from inferior pulvinar lesions may be dependent in part on visual attentional factors.

Visual and somatosensory receptive fields of neurons in the squirrel monkey pulvinar

Visual and somatosensory responses were studied in 329 neurons in the pulvinar of the squirrel monkey. Almost all somatosensory neurons (total= 46) in pulvinar lateralis (PL); most had continuous peripheral fields, though a few were bilaterally activated. Visual neurons (total= 179) were found in PL, pulvinar inferior (PI) and pulvinar medialis (PM). Of these, 29 responded only to diffuse illumination, while 150 had definable receptive fields. Approximately twice as many neurons in PI were responsive to light than neurons in PL or PM. The majority of visual units was responsive to some form of moving stimulus, and for some neurons there were additional specificities for directionality and orientation. Most visual neurons were monocularly driven (75%); nearly all visual units which could be mapped had receptive fields within 25° of the fovea. The majority of fields was in the visual hemifield contralateral to the recording electrode. Most visual neurons had receptive fields of at least 100 sq. degrees in area. A third group of 104 neurons was found unresponsive to visual and somatosensory stimuli.

Ultrastructure of the pulvinar of the squirrel monkey.

AbstractThree divisions of the squirrel monkey pulvinar, p. inferior (PI), p. lateralis (PL), and p. medialis (PM), have been studied with light‐ and electron‐microscopic techniques. Two populations of neurons exist. The first neuron is a thalamocortical relay cell (TCR), averaging about 26 μ in diameter, with radial dendritic pattern and thin dendritic appendages. The second is a Golgi type II neuron, about 16 μ average diameter, with more complex dendritic appendages and an axon ramifying in the vicinity of the soma. The TCR: Golgi type II ratio is about 7:3 in PL and PI, and 9:2 in PM.Three types of synaptic terminals are observed: the RS, comprising about 80% of the total population; the RL, comprising about 10%; and the F, comprising about 10%. The first two contain round vesicles and make asymmetrical synaptic contacts, while the third contains both round and flat vesicles and makes symmetrical synaptic contacts. Characteristic groupings of synaptic terminals and dendrites, called “glomeruli”, appear to be organized for structured and efficient interactions. Adhesive contacts are observed between synaptic and non‐synaptic and non‐synaptic structures.Comparisons with other thalamic nuclei are made, and the ultrastructural resemblance among all thalamic nuclei studied thus far is noted. The presence of glomeruli in all is discussed.