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Saccadic inhibition during free viewing in macaque monkeys

Orczyk, John J; Barczak, Annamaria; O'Connell, Monica N; Kajikawa, Yoshinao
Through the process of saccadic inhibition, visual events briefly suppress eye movements including microsaccades. In humans, saccadic inhibition has been shown to occur in response to the presentation of parafoveal or peripheral visual distractors during fixation and target-directed saccades and to physical changes of behaviorally relevant visual objects. In monkeys performing tasks that controlled eye movements, saccadic inhibition of microsaccades and target-directed saccades has been shown. Using eye data from three previously published studies, we investigated how saccade rate changed while monkeys were presented with visual stimuli under conditions with loose or no viewing demands. In two conditions, animals passively sat while an LED lamp flashed or screen-wide images appeared in front of them. In the third condition, images were repeated semiperiodically while animals had to maintain their gaze within a wide rectangular area and detect oddballs. Despite animals not being required to maintain fixation or make saccades to particular targets, the onset of visual events led to a temporary reduction of saccade rate across all conditions. Interestingly, saccadic inhibition was found at image offsets as well. These results show that saccadic inhibition occurs in monkeys during free viewing.NEW & NOTEWORTHY We investigated the time courses of saccade rate following visual stimuli during three conditions of free viewing in macaque monkeys. Under all conditions, saccade rate decreased transiently after the onset of visual stimuli. These results suggest that saccadic inhibition occurs during free viewing.
PMID: 36629324
ISSN: 1522-1598
CID: 5419042

Magnifying Traveling Waves on the Scalp

Orczyk, John J; Kajikawa, Yoshinao
Traveling waves appear in various signals that measure neuronal activity. Some signals measured in animals have singles-cell resolution and directly point to neuronal activity. In those cases, activation of distributed neurons forms a wave front, and the front propagates across the cortical surface. Other signals are variants of neuroelectric potentials, i.e. electroencephalography, electrocorticography and field potentials. Instead of having fine spatial resolution, these signals reflect the activity of neuronal populations via volume conduction (VC). Sources of traveling waves in neuroelectric potentials have not been well addressed so far. As animal studies show propagating activation of neurons that spread in measured areas, it is often considered that neuronal activations during scalp waves have similar trajectories of activation, spreading like scalp waves. However, traveling waves on the scalp differ from those found directly on the cortical surface in several dimensions: traveling velocity, traveling distance and areal size occupied by single polarity. We describe that the simplest sources can produce scalp waves with perceived spatial dimensions which are actually a magnification of neuronal activity emanating from local sources due to VC. This viewpoint is not a rigorous proof of our magnification concept. However, we suggest the possibility that the actual dimensions of neuronal activity producing traveling waves is not as large as the dimension of the traveling waves.
PMID: 34086189
ISSN: 1573-6792
CID: 4892132

Cross laminar traveling components of field potentials due to volume conduction of non-traveling neuronal activity in macaque sensory cortices

Orczyk, John J; Barczak, Annamaria; Costa-Faidella, Jordi; Kajikawa, Yoshinao
Field potentials (FP) reflect neuronal activities in the brain, and often exhibit traveling peaks across recording sites. While traveling FPs are interpreted as propagation of neuronal activity, not all studies directly reveal such propagating patterns of neuronal activation. Neuronal activity is associated with transmembrane currents that form dipoles and produce negative and positive fields. Thereby, FP components reverse polarity between those fields and have minimal amplitudes at the center of dipoles. Although their amplitudes could be smaller, FPs are never flat even around these reversals. What occurs around the reversal has not been addressed explicitly, even though those are rationally in the middle of active neurons. We show that sensory FPs around the reversal appeared with peaks traveling across cortical laminae in macaque sensory cortices. Interestingly, analyses of current source density (CSD) did not depict traveling patterns but lamina-delimited current sinks and sources. We simulated FPs produced by volume conduction of a simplified 2 dipoles' model mimicking sensory cortical laminar CSD components. While FPs generated by single dipoles followed the temporal patterns of the dipole moments without traveling peaks, FPs generated by concurrently active dipole moments appeared with traveling components in the vicinity of dipoles by superimposition of individually non-traveling FPs generated by single dipoles. These results indicate that not all traveling FP are generated by traveling neuronal activity, and that recording positions need to be taken into account to describe FP peak components around active neuronal populations.SIGNIFICANCE STATEMENTField potentials (FPs) are generated by neuronal activity in the brain occur with fields of opposite polarity. Likewise, in the cerebral cortices, they have mirror-imaged waveforms in upper and lower layers. We show that FPs appear like traveling across the cortical layers. Interestingly, the traveling FPs occur without traveling components of current source density (CSD), which represents transmembrane currents associated with neuronal activity. These seemingly odd findings are explained using CSD models of multiple dipoles. Concurrently active, non-traveling dipoles produce FPs as mixtures of FPs produced by individual dipoles, and result in traveling FP waveforms as the mixing ratio depends on the distances from those dipoles. The results suggest that not all traveling FP components are associated with propagating neuronal activity.
PMID: 34321312
ISSN: 1529-2401
CID: 4949812

Comparison of Scalp ERP to Faces in Macaques and Humans

Orczyk, John; Schroeder, Charles E; Abeles, Ilana Y; Gomez-Ramirez, Manuel; Butler, Pamela D; Kajikawa, Yoshinao
Face recognition is an essential activity of social living, common to many primate species. Underlying processes in the brain have been investigated using various techniques and compared between species. Functional imaging studies have shown face-selective cortical regions and their degree of correspondence across species. However, the temporal dynamics of face processing, particularly processing speed, are likely different between them. Across sensory modalities activation of primary sensory cortices in macaque monkeys occurs at about 3/5 the latency of corresponding activation in humans, though this human simian difference may diminish or disappear in higher cortical regions. We recorded scalp event-related potentials (ERPs) to presentation of faces in macaques and estimated the peak latency of ERP components. Comparisons of latencies between macaques (112 ms) and humans (192 ms) suggested that the 3:5 ratio could be preserved in higher cognitive regions of face processing between those species.
PMID: 33967709
ISSN: 1662-5137
CID: 4867082

Dissociation of broadband high-frequency activity and neuronal firing in the neocortex

Leszczyński, Marcin; Barczak, Annamaria; Kajikawa, Yoshinao; Ulbert, Istvan; Falchier, Arnaud Y; Tal, Idan; Haegens, Saskia; Melloni, Lucia; Knight, Robert T; Schroeder, Charles E
Broadband high-frequency activity (BHA; 70 to 150 Hz), also known as "high gamma," a key analytic signal in human intracranial (electrocorticographic) recordings, is often assumed to reflect local neural firing [multiunit activity (MUA)]. As the precise physiological substrates of BHA are unknown, this assumption remains controversial. Our analysis of laminar multielectrode data from V1 and A1 in monkeys outlines two components of stimulus-evoked BHA distributed across the cortical layers: an "early-deep" and "late-superficial" response. Early-deep BHA has a clear spatial and temporal overlap with MUA. Late-superficial BHA was more prominent and accounted for more of the BHA signal measured near the cortical pial surface. However, its association with local MUA is weak and often undetectable, consistent with the view that it reflects dendritic processes separable from local neuronal firing.
PMID: 32851172
ISSN: 2375-2548
CID: 4575762

Primary Generators of Visually Evoked Field Potentials Recorded in the Macaque Auditory Cortex

Kajikawa, Yoshinao; Smiley, John F; Schroeder, Charles E
Prior studies have reported "local" field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be "contaminated" by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such "far-field" activity, in addition to, or in absence of, local synaptic responses.SIGNIFICANCE STATEMENT Field potentials (FPs) can index neuronal population activity that is not evident in action potentials. However, due to volume conduction, FPs may reflect activity in distant neurons superimposed upon that of neurons close to the recording electrode. This is problematic as the default assumption is that FPs originate from local activity, and thus are termed "local" (LFP). We examine this general problem in the context of previously reported face-evoked FPs in macaque auditory cortex. Our findings suggest that face-FPs are indeed generated in the underlying inferotemporal cortex and volume-conducted to the auditory cortex. The note of caution raised by these findings is of particular importance for studies that seek to assign FP/LFP recordings to specific cortical layers.
PMID: 28924008
ISSN: 1529-2401
CID: 3068542

Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates

Qi, Hui-Xin; Reed, Jamie L; Franca, Joao G; Jain, Neeraj; Kajikawa, Yoshinao; Kaas, Jon H
In somatosensory cortex, tactile stimulation within the neuronal receptive field (RF) typically evokes a transient excitatory response with or without postexcitatory inhibition. Here, we describe neuronal responses in which stimulation on the hand is followed by suppression of the ongoing discharge. With the use of 16-channel microelectrode arrays implanted in the hand representation of primary somatosensory cortex of New World monkeys and prosimian galagos, we recorded neuronal responses from single units and neuron clusters. In 66% of our sample, neuron activity tended to display suppression of firing when regions of skin outside of the excitatory RF were stimulated. In a small proportion of neurons, single-site indentations suppressed firing without initial increases in response to any of the tested sites on the hand. Latencies of suppressive responses to skin indentation (usually 12-34 ms) were similar to excitatory response latencies. The duration of inhibition varied across neurons. Although most observations were from anesthetized animals, we also found similar neuron response properties in one awake galago. Notably, suppression of ongoing neuronal activity did not require conditioning stimuli or multi-site stimulation. The suppressive effects were generally seen following single-site skin indentations outside of the neuron's minimal RF and typically on different digits and palm pads, which have not often been studied in this context. Overall, the characteristics of widespread suppressive or inhibitory response properties with and without initial facilitative or excitatory responses add to the growing evidence that neurons in primary somatosensory cortex provide essential processing for integrating sensory stimulation from across the hand.
PMID: 26912593
ISSN: 1522-1598
CID: 4102202

Predictive motor control of sensory dynamics in auditory active sensing

Morillon, Benjamin; Hackett, Troy A; Kajikawa, Yoshinao; Schroeder, Charles E
Neuronal oscillations present potential physiological substrates for brain operations that require temporal prediction. We review this idea in the context of auditory perception. Using speech as an exemplar, we illustrate how hierarchically organized oscillations can be used to parse and encode complex input streams. We then consider the motor system as a major source of rhythms (temporal priors) in auditory processing, that act in concert with attention to sharpen sensory representations and link them across areas. We discuss the circuits that could mediate this audio-motor interaction, notably the potential role of the somatosensory system. Finally, we reposition temporal predictions in the context of internal models, discussing how they interact with feature-based or spatial predictions. We argue that complementary predictions interact synergistically according to the organizational principles of each sensory system, forming multidimensional filters crucial to perception.
PMID: 25594376
ISSN: 1873-6882
CID: 4102192

Auditory properties in the parabelt regions of the superior temporal gyrus in the awake macaque monkey: an initial survey

Kajikawa, Yoshinao; Frey, Stephen; Ross, Deborah; Falchier, Arnaud; Hackett, Troy A; Schroeder, Charles E
The superior temporal gyrus (STG) is on the inferior-lateral brain surface near the external ear. In macaques, 2/3 of the STG is occupied by an auditory cortical region, the "parabelt," which is part of a network of inferior temporal areas subserving communication and social cognition as well as object recognition and other functions. However, due to its location beneath the squamous temporal bone and temporalis muscle, the STG, like other inferior temporal regions, has been a challenging target for physiological studies in awake-behaving macaques. We designed a new procedure for implanting recording chambers to provide direct access to the STG, allowing us to evaluate neuronal properties and their topography across the full extent of the STG in awake-behaving macaques. Initial surveys of the STG have yielded several new findings. Unexpectedly, STG sites in monkeys that were listening passively responded to tones with magnitudes comparable to those of responses to 1/3 octave band-pass noise. Mapping results showed longer response latencies in more rostral sites and possible tonotopic patterns parallel to core and belt areas, suggesting the reversal of gradients between caudal and rostral parabelt areas. These results will help further exploration of parabelt areas.
PMID: 25762661
ISSN: 1529-2401
CID: 4087272

Generation of field potentials and modulation of their dynamics through volume integration of cortical activity

Kajikawa, Yoshinao; Schroeder, Charles E
Field potentials (FPs) recorded within the brain, often called "local field potentials" (LFPs), are useful measures of net synaptic activity in a neuronal ensemble. However, due to volume conduction, FPs spread beyond regions of underlying synaptic activity, and thus an "LFP" signal may not accurately reflect the temporal patterns of synaptic activity in the immediately surrounding neuron population. To better understand the physiological processes reflected in FPs, we explored the relationship between the FP and its membrane current generators using current source density (CSD) analysis in conjunction with a volume conductor model. The model provides a quantitative description of the spatiotemporal summation of immediate local and more distant membrane currents to produce the FP. By applying the model to FPs in the macaque auditory cortex, we have investigated a critical issue that has broad implications for FP research. We have shown that FP responses in particular cortical layers are differentially susceptible to activity in other layers. Activity in the supragranular layers has the strongest contribution to FPs in other cortical layers, and infragranular FPs are most susceptible to contributions from other layers. To define the physiological processes generating FPs recorded in loci of relatively weak synaptic activity, strong effects produced by synaptic events in the vicinity have to be taken into account. While outlining limitations and caveats inherent to FP measurements, our results also suggest specific peak and frequency band components of FPs can be related to activity in specific cortical layers. These results may help improving the interpretability of FPs.
PMID: 25274348
ISSN: 1522-1598
CID: 4102182