Action Categorization in Rhesus Monkeys: discrimination of grasping from non-grasping manual motor acts

The ability to recognize others’ actions is an important aspect of social behavior. While neurophysiological and behavioral research in monkeys has offered a better understanding of how the primate brain processes this type of information, further insight with respect to the neural correlates of action recognition requires tasks that allow recording of brain activity or perturbing brain regions while monkeys simultaneously make behavioral judgements about certain aspects of observed actions. Here we investigated whether rhesus monkeys could actively discriminate videos showing grasping or non-grasping manual motor acts in a two-alternative categorization task. After monkeys became proficient in this task, we tested their ability to generalize to a number of untrained, novel videos depicting grasps or other manual motor acts. Monkeys generalized to a wide range of novel human or conspecific grasping and non-grasping motor acts. They failed, however, for videos showing unfamiliar actions such as a non-biological effector performing a grasp, or a human hand touching an object with the back of the hand. This study shows the feasibility of training monkeys to perform active judgements about certain aspects of observed actions, instrumental for causal investigations into the neural correlates of action recognition

Intrinsic functional clustering of ventral premotor F5 in the macaque brain

© 2020 Neurophysiological and anatomical data suggest the existence of several functionally distinct regions in the lower arcuate sulcus and adjacent postarcuate convexity of the macaque monkey. Ventral premotor F5c lies on the postarcuate convexity and consists of a dorsal hand-related and ventral mouth-related field. The posterior bank of the lower arcuate contains two additional premotor F5 subfields at different anterior-posterior levels, F5a and F5p. Anterior to F5a, area 44 has been described as a dysgranular zone occupying the deepest part of the fundus of the inferior arcuate. Finally, area GrFO occupies the most rostral portion of the fundus and posterior bank of inferior arcuate and extends ventrally onto the frontal operculum. Recently, data-driven exploratory approaches using resting-state fMRI data have been suggested as a promising non-invasive method for examining the functional organization of the primate brain. Here, we examined to what extent partitioning schemes derived from data-driven clustering analysis of resting-state fMRI data correspond with the proposed organization of the fundus and posterior bank of the macaque arcuate sulcus, as suggested by invasive architectonical, connectional and functional investigations. Using a hierarchical clustering analysis, we could retrieve clusters corresponding to the dorsal and ventral portions of F5c on the postarcuate convexity, F5a and F5p at different antero-posterior locations on the posterior bank of the lower arcuate, area 44 in the fundus, as well as part of area GrFO in the most anterior portion of the fundus. Additionally, each of these clusters displayed distinct whole-brain functional connectivity, in line with previous anatomical tracer and seed-based functional connectivity investigations of F5/44 subdivisions. Overall, our data suggests that hierarchical clustering analysis of resting-state fMRI data can retrieve a fine-grained level of cortical organization that resembles detailed parcellation schemes derived from invasive functional and anatomical investigations

The Extraction of Depth Structure from Shading and Texture in the Macaque Brain

We used contrast-agent enhanced functional magnetic resonance imaging (fMRI) in the alert monkey to map the cortical regions involved in the extraction of 3D shape from the monocular static cues, texture and shading. As in the parallel human imaging study [1], we contrasted the 3D condition to several 2D control conditions. The extraction of 3D shape from texture (3D SfT) involves both ventral and parietal regions, in addition to early visual areas. Strongest activation was observed in CIP, with decreasing strength towards the anterior part of the intraparietal sulcus (IPS). In the ventral stream 3D SfT sensitivity was observed in a ventral portion of TEO. The extraction of 3D shape from shading (3D SfS) involved predominantly ventral regions, such as V4 and a dorsal potion of TEO. These results are similar to those obtained earlier in human subjects and indicate that the extraction of 3D shape from texture is performed in both ventral and dorsal regions for both species, as are the motion and disparity cues, whereas shading is mainly processed in the ventral stream

Retinotopic mapping in awake monkeys suggests a different functional organization for dorsal and ventral V4

Using functional magnetic resonance imaging, we mapped the retinotopic organization throughout the visual cortex of fixating monkeys. The observed retinotopy in V1, V2 and V3 was completely consistent with the classical view. More rostrally in occipital cortex, both areas V3A and MT/V5 had a lower and upper visual field representation split by a horizontal meridian. Both areas were almost completely surrounded by a vertical meridian representa- tion. Ventral, but not dorsal V4 was rostrally bordered by a horizontal meridian. Furthermore, contrary to all other early visual areas including V4v, the eccentricity lines ran almost parallel to the areal boundaries in V4d. These results suggest a different functional organization in dorsal and ventral V4, similar to what has been observed in human

Functional anatomy of visual processing in the cerebral cortex of the macaque.

In deze doctoraatsthesis werd onderzocht welke gebieden in de hersenschors bij de aap, bijdragen in het verwerken van kleur en visuele bewegingsinformatie. Verder werd onderzocht welke gebieden tussenkomen in het begrijpen van gedragingen of acties van andere personen. Het doel was om tot een beter inzicht te komen van de functionele organisatie van de hersenschors bij de aap. Deze studies werden uitgevoerd door middel van twee functionele beeldvormingstechnieken, de dubbel-label deoxyglucose techniek (DG) en functionele magnetische resonantie beeldvorming (fMRI) bij de wakkere aap (Hoofdstuk 2). Beide technieken laten toe om een beeld te krijgen van stimulus-gerelateerde neuronale activiteit in gans de hersenen over een beperkte tijdsperiode. De resultaten van de kleur-experimenten (Hoofdstuk 3) toonden duidelijk aan dat informatie omtrent de kleur van een stimulus, verwerkt wordt in een groep van hersengebieden die allen deel uitmaken van de ventrale baan dewelke instaat voor de perceptie van objecten. Kleur-gerelateerde activiteit werd in visuele gebieden V1, V2, V3, V4 en inferio-temporele cortex (gebied TEO en TE) waargenomen. Deze bevindingen zijn niet in overeenstemming met vroegere controversiële beweringen dat kleurinformatie verwerkt wordt in slechts 1 extrastriaat gebied (met name V4; Zeki SM, Brain Res 1973 53: 422-427) en tonen het nut aan van technieken die functionele activiteit in gans de cortex kunnen registreren, als een complementaire techniek voor de single cell metingen. In hoofdstuk 4 onderzochten we welke gebieden in de superior temporele sulcus (STS) van de aap een rol spelen in de analyse van bewegende stimuli. Terwijl het caudale gedeelte van de STS, met inbegrip van gebieden MT/V5 en MST, veelvuldig bestudeerd is, is er eigenlijk relatief weinig geweten van de rol die de meer anterio-ventraal gelegen STS gebieden spelen in de analyse van bewegende stimuli. Met behulp van fMRI zijn we erin geslaagd om zes verschillende bewegingsgevoelige gebieden te localiseren en af te lijnen in de STS. Eén hiervan, een gebied dat we LST (lower superior temporal) genoemd hebben, was tot nu toe niet beschreven als bewegingsgevoelig gebied. Met behulp van een groot aantal bewegingstesten hebben we de zes gebieden verder functioneel kunnen karakteriseren en konden we besluiten dat bewegings-gerelateerde informatie mogelijks via twee banen wordt verwerkt in de STS. Een eerste, caudale baan die gebieden MT/V5 en MST omvat is betrokken bij het berekenen van de richting waarin wij ons begeven als we ons verplaatsen. Een tweede baan, die de meer rostrale bewegingsgevoelige gebieden FST, LST en STPm omvat, is mogelijks betrokken in het verwerken van visuele informatie omtrent biologische bewegingen (bewegingen van levende objecten) en acties. Tot slot onderzochten we hoe en waar in de hersenen visuele informatie omtrent acties van anderen wordt verwerkt (Hoofdstuk 5 en 6). Zo vonden we ondermeer in hoofdstuk 5, dat het observeren van grijpbewegingen uitgevoerd door een persoon, verscheidene gebieden activeert in de premotor cortex van de aap. Opmerkelijk is dat deze premotor gebieden voornamelijk een motoriële functie hebben, namelijk het uitvoeren van diverse hogere orde motor handelingen (bv. vastgrijpen van een object). Deze resultaten bevestigen de stelling dat we acties van anderen kunnen begrijpen doordat het observeren van een bepaalde beweging van iemand anders onze eigen motor representatie van diezelfde beweging activeert. Verder toonden deze studies aan dat er in de frontale cortex van de aap een onderscheid wordt gemaakt tussen context-afhankelijke (een persoon die grijpt) en meer abstracte (een hand die grijpt) actie representaties. In hoofdstuk 6 bestudeerden we twee andere gebieden waarvan reeds was aangetoond dat ze een rol spelen in het verwerken van visuele informatie omtrent acties van anderen, de reeds eerder genoemde superior temporele sulcus (STS) en de pariëtale cortex. In de pariëtale cortex vonden we eenzelfde onderscheid tussen enerzijds context-afhankelijke en anderzijds meer abstracte actie representaties. Deze resultaten tonen aan dat de parietale cortex niet enkel visuele informatie verwerkt nodig voor motor organisatie, maar eveneens een rol spelen in de visuele verwerking van acties. Op basis van enerzijds anatomische connecties tussen de STS, pariëtale en frontale cortex, en anderzijds bewegings-, vorm- en actie-gerelateerde activiteit in de 3 eerder vermelde gebieden, suggeerden we tentatief hoe visuele informatie omtrent acties vanuit de STS naar de frontale cortex kan worden gestuurd via drie verschillende banen. Deze laatste werkhypothese zal in de toekomst getest worden door bijkomend fMRI controle experimenten en combinatie van fMRI, inactivatie en microstimulatie experimenten terwijl apen een grijpbeweging uitvoeren ofwel naar kijken naar grijpbewegingen uitgevoerd door anderen.status: publishe

Action recognition in the primate brain: a comparative functional MRI study of the organization and function of human mirror system and non-human primate.

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FMRI responses in non-human primate somatosensory cortex during grasp and touch observation

Background: Numerous studies in human and non-human primates have shown that merely observing other's actions can modulate activity in the observer's motor cortices. Similar automatic responses have also been suggested in human somatosensory cortices when actions involving touch are observed, with some studies suggesting an involvement of primary S1 (Pihko et al., 2010) and/or secondary S2 somatosensory regions (Keysers et al., 2004), while others emphasize the involvement of more posterior parietal regions (Chan and Baker, 2015). Methods: Here we investigated brain responses during grasp or mere touch observation using contrast-enhanced functional MRI (Siemens 3 Tesla) in monkeys. We first localized hand representations of S1 and S2 in three macaques (male, 4-6 kg) by stimulating the hand region with a brush in anaesthetized fMRI scans. In subsequent awake experiments, we scanned these monkeys while they observed videos of various actions displaying different instances of touch (grasping or simple touching of objects or hands). Control videos depicted the same actors performing reaching movements towards the same objects/hands without interacting with them. In an additional experiment, videos of different actions (grasp and touch) towards a hand displaying obvious skin displacements (Ferri et al., 2015) were also presented. Results: A region-of-interest analysis of S1 and S2 hand regions responding during passive tactile stimulation did not yield significant fMRI signal increases during either grasp or touch observation (compared to controls), nor did observing actions showing obvious skin displacements. Posterior parietal regions, including AIP and PFG, as well as premotor F5, in addition to early visual and STS regions, showed significant responses during observation of both grasp and mere touch (compared to controls). Interestingly, a more anterior S2 sector, that mainly responds during monkeys' active hand manipulation tasks like grasp execution (Nelissen and Vanduffel., 2011; Ishida et al., 2013), showed consistent responses during touch observation, particular those actions involving a grasp. Conclusion: Our results suggest that somatosensory sectors of monkey S1 and S2 that respond significantly during passive tactile stimulation do not show modulations during grasp and touch observation. However, a more anterior portion of S2 responds during touch observation. These observations are in line with recent evidence of single-cell responses in macaque S2 during human action observation (Hihara et al., 2015). Functional MRI responses in monkey somatosensory cortex during grasp and touch ob... Page 1 of 1 http://status: publishe

Motor resonance in monkey parietal and premotor cortex during action observation: influence of viewing perspective and effector identity

Observing others performing motor acts like grasping has been shown to elicit neural responses in the observer`s parieto-frontal motor network, which typically becomes active when the observer would perform these actions him/herself. While some human studies suggested strongest motor resonance during observation of first person or egocentric perspectives compared to third person or allocentric perspectives, other research either report the opposite or did not find any viewpoint-related preferences in parieto-premotor cortices. Furthermore, it has been suggested that these motor resonance effects are lateralized in the parietal cortex depending on the viewpoint and identity of the observed effector (left vs right hand). Other studies, however, do not find such straightforward hand identity dependent motor resonance effects. In addition to these conflicting findings in human studies, to date, little is known about the modulatory role of viewing perspective and effector identity (left or right hand) on motor resonance effects in monkey parieto-premotor cortices. Here, we investigated the extent to which different viewpoints of observed conspecific hand actions yield motor resonance in rhesus monkeys using fMRI. Observing first person, lateral and third person viewpoints of conspecific hand actions yielded significant activations throughout the so-called action observation network, including STS, parietal and frontal cortices. Although region-of-interest analysis of parietal and premotor motor/mirror neuron regions AIP, PFG and F5, showed robust responses in these regions during action observation in general, a clear preference for egocentric or allocentric perspectives was not evident. Moreover, except for lateralized effects due to visual field biases, motor resonance in the monkey brain during grasping observation did not reflect hand identity dependent coding.status: Published onlin