Directed information exchange between cortical layers in macaque V1 and V4 and its modulation by selective attention

Ferro, Demetrio; Kempen, Jochem van; Boyd, Michael; Panzeri, Stefano; Thiele, Alexander

doi:10.1073/pnas.2022097118

Cited by 62 publications

(70 citation statements)

References 85 publications

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“…The increase in p s , on the other hand, is consistent with the observation that interactions between cortical layers in V4 increase during attention 43 . The increase in p s can be counterbalanced by a reduction in p r mediated by neuromodulatory effects that reduce the efficacy of lateral connections in the cortex during attention 44 .…”

Section: Resultssupporting

confidence: 89%

“…These feedback inputs can coordinate activity across minicolumns in V4. Moreover, vertical interactions in V4 measured with local field potentials (LFPs) increase during attention 43 , while neuromodulatory mechanisms can reduce horizontal interactions. The level of Acetylcholine (ACh) can modify the efficacy of synaptic interactions during attention in a selective manner 44 .…”

Section: Discussionmentioning

confidence: 99%

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Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity

Zeraati

Shi

Steinmetz

et al. 2021

Preprint

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Neural activity fluctuates endogenously on timescales varying across the neocortex. The variation in these intrinsic timescales relates to the functional specialization of cortical areas and their involvement in the temporal integration of information. Yet, it is unknown whether the timescales can adjust rapidly and selectively to the demands of a cognitive task. We measured intrinsic timescales of local spiking activity within columns of area V4 while monkeys performed spatial attention tasks. The ongoing spiking activity unfolded across at least two distinct timescales---fast and slow---and the slow timescale increased when monkeys attended to the receptive fields location. A recurrent network model shows that multiple timescales in local dynamics arise from spatial connectivity mimicking vertical and horizontal interactions in visual cortex and that slow timescales increase with the efficacy of recurrent interactions. Our results reveal that targeted neural populations integrate information over variable timescales following the demands of a cognitive task and propose an underlying network mechanism.

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Section: Resultssupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity

Zeraati

Shi

Steinmetz

et al. 2021

Preprint

Self Cite

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“…In this paper we have mainly focused on the interactions between two neuronal groups oscillating in the gamma range, but we have not discussed the interaction of gamma with other rhythms, namely beta (13-30 Hz), alpha (8-13 Hz) and theta (4-8 Hz) [35,37]. The interplay between different frequency rhythms may definitely have an important role for communication and cognition [37,9,48,49,50] and the methods discussed herein may contribute to unveil possible mechanisms. Namely, a thorough study of the solutions emerging in the p:1 phase-locking regions, where the input is p times slower than the intrinsic oscillatory frequency.…”

Section: Discussionmentioning

confidence: 99%

Phase-locking patterns underlying effective communication in exact firing rate models of neural networks

Reyner-Parra

Huguet

2021

Preprint

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Macroscopic oscillations in the brain have been observed to be involved in many cognitive tasks but their role is not completely understood. One of the suggested functions of the oscillations is to dynamically modulate communication between neural circuits. The Communication Through Coherence (CTC) theory establishes that oscillations reflect rhythmic changes in excitability of the neuronal populations. Thus, populations need to be properly phase-locked so that input volleys arrive at the peaks of excitability of the receiving population to communicate effectively. Here, we present a modeling study to explore synchronization between neuronal circuits connected with unidirectional projections. We consider an Excitatory-Inhibitory (E-I) network of quadratic integrate-and-fire neurons modeling a Pyramidal-Interneuronal Network Gamma (PING) rhythm. The network receives an external periodic input from either one or two sources, simulating the inputs from other oscillating neural groups. We use recently developed mean-field models which provide an exact description of the macroscopic activity of the spiking network. This low-dimensional mean field model allows us to use tools from bifurcation theory to identify the phase-locked states between the input and the target population as a function of the amplitude, frequency and coherence of the inputs. We identify the conditions for optimal phaselocking and selective communication. We find that inputs with high coherence can entrain the network for a wider range of frequencies. Besides, faster oscillatory inputs than the intrinsic network gamma cycle show more effective communication than inputs with similar frequency. Our analysis further shows that the entrainment of the network by inputs with higher frequency is more robust to distractors, thus giving them an advantage to entrain the network. Finally, we show that pulsatile inputs can switch between attended inputs in selective attention.

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“…The main task and stimuli have been described previously (Ferro et al, 2021;Thiele et al, 2016;van Kempen et al, 2021). In brief, the monkey initiated a trial by holding a lever and fixating a white fixation spot (0.1°) displayed on a grey background (1.41 cd/m 2 ).…”

Section: Behavioral Paradigmsmentioning

confidence: 99%

Dopamine influences attentional rate modulation in Macaque posterior parietal cortex

Kempen

Brandt

Distler

et al. 2020

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Selective attention facilitates the prioritization of task-relevant sensory inputs over those which are irrelevant. Although cognitive neuroscience has made great strides in understanding the neural substrates of attention, our understanding of its neuropharmacology is incomplete. Cholinergic and glutamatergic contributions have been demonstrated, but emerging evidence also suggests an important influence of dopamine (DA). DA has historically been investigated in the context of frontal/prefrontal function arguing that dopaminergic receptor density in the posterior/parietal cortex is sparse. However, this notion was derived from rodent data, whereas in primates DA innervation in parietal cortex matches that of many prefrontal areas. We recorded single- and multi-unit activity whilst iontophoretically administering dopaminergic agonists and antagonists to posterior parietal cortex of rhesus macaques engaged in a spatial attention task. Out of 88 neurons, 50 showed modulation of activity induced by drug administration. Dopamine inhibited firing rates across the population according to an inverted-U shaped dose-response curve. D1 receptor antagonists diminished firing rates in broad-spiking units according to a monotonically increasing function. Additionally, dopamine modulated attentional signals in broad, but not narrow-spiking cells. Finally, both drugs modulated the pupil light reflex. These data show that dopamine plays an important role in shaping neuronal responses and modulates attentional processing in macaque parietal cortex.Significance statementDopamine is critically involved in high-level cognitive functions, and dopaminergic dysfunctions pertain to ageing and neurological and psychiatric disorders. Most previous studies focused on dopaminergic effects on prefrontal activity or its role in basal ganglia circuitry. The effects of dopamine in other brain areas such as parietal cortex, despite its well-established role in cognition and cognitive dysfunction, have largely been overlooked. This study is the first to show dopaminergic modulation of parietal activity in general, and specific to spatial attention in the non-human primate, revealing cell-type specific effects of dopamine on attentional modulation.

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Directed information exchange between cortical layers in macaque V1 and V4 and its modulation by selective attention

Cited by 62 publications

References 85 publications

Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity

Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity

Phase-locking patterns underlying effective communication in exact firing rate models of neural networks

Dopamine influences attentional rate modulation in Macaque posterior parietal cortex

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