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Biology subjects

Afraz, A.

Publications and source records attributed to Afraz, A..

7 recordsLinked to original sources

Inferotemporal cortex stimulation is perceived before its onset

Neural response latency measures when stimulus-evoked activity becomes detectable, but it does not reveal when the brain assigns the causal contribution of that activity to events in the external world. We define this temporal adjustment as projected delay and measure it in the macaque inferotemporal cortex using optogenetic stimulation and behavior. Two rhesus macaques performed a cortical perturbation detection task in which a visual masker appeared at different times relative to stimulation. Detection was selectively impaired when the masker began 200 ms before stimulation. We then tested this timing using Perceptography, a method that optimizes image perturbations to mimic stimulation-evoked visual events. Image perturbations presented 200 ms before stimulation elicited higher false-alarm rates than perturbations presented at stimulation onset. Here, we show that stimulation-evoked visual events in inferotemporal cortex depend preferentially on visual information originating approximately 200 ms before the cortical perturbation. This projected delay exceeds typical inferotemporal response latencies and suggests temporally extended readout mechanisms relevant to causal models of visual perception and the timing of cortical visual prostheses.

neuroscience↗

3D-Printable Non-invasive Head Immobilization System for Non-Human Primates

A critical contribution to understanding the primate brain is our ability to directly record, manipulate, or image the brain in awake, behaving monkeys. A challenge with carrying out these studies is that typically the monkeys head must be fixed in place. While non-invasive head immobilization systems (NHIS) have been demonstrated to be effective, they have not fully replaced the use of surgically applied headposts. Here, we introduce a novel NHIS, with an option for voluntary engagement, for macaques using a widely available resource: the 3D printer. We designed customized 3D-printable head-immobilization masks for monkeys and a docking system using standard CT scans and user-friendly open-source software packages (FLoRIN, Blender, Python). We examined the efficacy and stability of our mask system for collecting eye fixation data by measuring trial-by-trial gaze precision and accuracy in two mask-immobilized monkeys and three headposted monkeys, including a within-subjects comparison. Our results demonstrate that monkeys stabilized by the mask maintain gaze precision and accuracy comparable with their headposted counterparts. While the headpost outperformed the mask, the difference in precision was 0.03{degrees} of visual angle, and the difference in accuracy was less than 0.2{degrees}, well within the acceptable range for most use-cases. Our process allows for the production of 3D-printable masks based on CT or MRI scans with the flexibility to incorporate design modifications for experimental equipment and resizing, potentially serving as a promising and more easily accessible alternative to headposts and other NHISs for primate neuroscience research.

physiology↗

Inactivation of face selective neurons alters eye movements when free viewing faces

During free viewing, faces attract gaze and induce specific fixation patterns corresponding to the facial features. This suggests that neurons encoding the facial features are in the causal chain that steers the eyes. However, there is no physiological evidence to support a mechanistic link between face encoding neurons in high-level visual areas and the oculomotor system. In this study, we targeted the middle face patches of inferior temporal (IT) cortex in two macaque monkeys using an fMRI localizer. We then utilized muscimol microinjection to unilaterally suppress IT neural activity inside and outside the face patches and recorded eye movements while the animals free viewing natural scenes. Inactivation of the face selective neurons altered the pattern of eye movements on faces: the monkeys found faces in the scene but neglected the eye contralateral to the inactivation hemisphere. These findings reveal the causal contribution of the high-level visual cortex in eye movements. SignificanceIt has been shown, for more than half a century, that eye movements follow distinctive patterns when free viewing faces. This suggests causal involvement of the face-encoding visual neurons in the eye movements. However, the literature is scant of evidence for this possibility and has focused mostly on the link between low-level image saliency and eye movements. Here, for the first time, we bring causal evidence showing how face-selective neurons in inferior temporal cortex inform and steer eye movements when free viewing faces.

neuroscience↗

Behavioral detectability of optogenetic stimulation of inferior temporal cortex varies with the size of concurrently viewed objects.

We have previously demonstrated that macaque monkeys can behaviorally detect a subtle optogenetic impulse delivered to their inferior temporal (IT) cortex. We have also shown that the ability to detect the cortical stimulation impulse varies depending on some characteristics of the visual images viewed at the time of brain stimulation, revealing the visual nature of the perceptual events induced by stimulation of the IT cortex. Here we systematically studied the effect of the size of viewed objects on behavioral detectability of optogenetic stimulation of the central IT cortex. Surprisingly, we found that behavioral detection of the same optogenetic impulse highly varies with the size of the viewed object images. Reduction of the object size in four steps from 8 to 1 degree of visual angle significantly decreased detection performance. These results show that identical stimulation impulses delivered to the same neural population induce variable perceptual events depending on the mere size of the objects viewed at the time of brain stimulation.

neuroscience↗

Perceptography: unveiling visual perceptual hallucinations induced by optogenetic stimulation of the inferior temporal cortex.

Neurons in the inferotemporal (IT) cortex respond selectively to complex visual features, implying their role in object perception. However, perception is subjective and cannot be read out from neural responses; thus, bridging the causal gap between neural activity and perception demands independent characterization of perception. Historically though, the complexity of the perceptual alterations induced by artificial stimulation of IT cortex has rendered them impossible to quantify. Here we addressed this old problem by combining machine learning with high-throughput behavioral optogenetics in macaque monkeys. In closed-loop experiments, we generated complex and highly specific images that the animal could not discriminate from the state of being cortically stimulated. These images, named "perceptograms" for the first time, reveal and depict the contents of the complex hallucinatory percepts induced by local neural perturbation in IT cortex. Furthermore, we found that the nature and magnitude of these hallucinations highly depend on concurrent visual input, stimulation location, and intensity. Objective characterization of stimulation-induced perceptual events opens the door to developing a mechanistic theory of visual perception. Further, it enables us to make better visual prosthetic devices and gain a greater understanding of visual hallucinations in mental disorders. One-Sentence SummaryCombining state-of-the-art AI with high-throughput closed-loop brain stimulation experiments, for the first time, we took "pictures" of the complex and subjective visual hallucinations induced by local stimulation in the inferior temporal cortex, a cortical area associated with object recognition.

neuroscience↗

Surgical procedure for implantation of Opto-Array in nonhuman primates

Optogenetics allows precise temporal control of neuronal activity in the brain. Engineered viral vectors are routinely used to transduce neurons with light-sensitive opsins. However, reliable virus injection and light delivery in animals with large brains, such as nonhuman primates, has proven challenging. The Opto-Array is a novel yet simple device that is used to deliver light to extended regions of surface cortex for high-throughput behavioral optogenetics in large brains. Here we present protocols for surgical delivery of virus and implantation of the Opto-Array in two separate surgeries in a rhesus monkeys inferior temporal cortex. As a proof of concept, we measured the behavioral performance of an animal detecting cortical optogenetic stimulations with different illumination power and duration using the Opto-Array. The animal was able to detect the optogenetic stimulation for all tested illumination powers and durations. A regression analysis also showed both power and duration of illumination significantly modulate the detectability of the optogenetic stimulation. The outcome of this approach is superior to the standard practice of injecting and recording through a chamber for large areas of surface cortex. Moreover, the chronic nature of the Opto-Array allows perturbation of neuronal activity of the same site across multiple sessions because it is highly stable, thus data can be pooled over months. The detailed surgical method presented here makes it possible to use optogenetics to modulate neuronal activity across large regions of surface cortex in the nonhuman primate brain.

neuroscience↗

Chronically implantable LED arrays for behavioral optogenetics in primates.

Challenges in behavioral optogenetics in large brains demand development of a chronically implantable platform for light delivery. We have developed Opto-Array, a chronically implantable array of LEDs for high-throughput optogenetic perturbation in non-human primates. We tested the Opto-Array in the primary visual cortex of a macaque monkey, and demonstrated that optogenetic cortical silencing by the Opto-Array results in reliable retinotopic visual deficits on a luminance discrimination task.

neuroscience↗