Layer and rhythm specificity for predictive routing

In predictive coding, experience generates predictions that attenuate the feeding forward of predicted stimuli while passing forward unpredicted “errors.” Different models have suggested distinct cortical layers, and rhythms implement predictive coding. We recorded spikes and local field potentials from laminar electrodes in five cortical areas (visual area 4 [V4], lateral intraparietal [LIP], posterior parietal area 7A, frontal eye field [FEF], and prefrontal cortex [PFC]) while monkeys performed a task that modulated visual stimulus predictability. During predictable blocks, there was enhanced alpha (8 to 14 Hz) or beta (15 to 30 Hz) power in all areas during stimulus processing and prestimulus beta (15 to 30 Hz) functional connectivity in deep layers of PFC to the other areas. Unpredictable stimuli were associated with increases in spiking and in gamma-band (40 to 90 Hz) power/connectivity that fed forward up the cortical hierarchy via superficial-layer cortex. Power and spiking modulation by predictability was stimulus specific. Alpha/beta power in LIP, FEF, and PFC inhibited spiking in deep layers of V4. Area 7A uniquely showed increases in high-beta (∼22 to 28 Hz) power/connectivity to unpredictable stimuli. These results motivate a conceptual model, predictive routing. It suggests that predictive coding may be implemented via lower-frequency alpha/beta rhythms that “prepare” pathways processing-predicted inputs by inhibiting feedforward gamma rhythms and associated spiking.

Layer and rhythm specificity for predictive routing

SummaryIn predictive coding, experience generates predictions that attenuate the feeding forward of predicted stimuli while passing forward unpredicted “errors”. Different models have different neural implementations of predictive coding. We recorded spikes and local field potentials from laminar electrodes in five cortical areas (V4, LIP, area 7A, FEF, and PFC) while monkeys performed a task that modulated visual stimulus predictability. Pre-stimulus predictions were associated with increased alpha/beta (8-30 Hz) power/coherence that fed back the cortical hierarchy primarily via deep-layer cortex. Unpredictable stimuli were associated with increases in spiking and in gamma-band (40-90 Hz) power/coherence that fed forward up the cortical hierarchy via superficial-layer cortex. Area 7A uniquely showed increases in high-beta (~22-28 Hz) power/coherence to unpredicted stimuli. These results suggest that predictive coding may be implemented via lower-frequency alpha/beta rhythms that “prepare” pathways processing predicted inputs by inhibiting feedforward gamma rhythms and associated spiking.

Visual and Vestibular Selectivity for Self-Motion in Macaque Posterior Parietal Area 7a

We examined the responses of neurons in posterior parietal area 7a to passive rotational and translational self-motion stimuli, while systematically varying the speed of visually simulated (optic flow cues) or actual (vestibular cues) self-motion. Contrary to a general belief that responses in area 7a are predominantly visual, we found evidence for a vestibular dominance in self-motion processing. Only a small fraction of neurons showed multisensory convergence of visual/vestibular and linear/angular self-motion cues. These findings suggest possibly independent neuronal population codes for visual versus vestibular and linear versus angular self-motion. Neural responses scaled with self-motion magnitude (i.e., speed) but temporal dynamics were diverse across the population. Analyses of laminar recordings showed a strong distance-dependent decrease for correlations in stimulus-induced (signal correlation) and stimulus-independent (noise correlation) components of spike-count variability, supporting the notion that neurons are spatially clustered with respect to their sensory representation of motion. Single-unit and multiunit response patterns were also correlated, but no other systematic dependencies on cortical layers or columns were observed. These findings describe a likely independent multimodal neural code for linear and angular self-motion in a posterior parietal area of the macaque brain that is connected to the hippocampal formation.

Speed tuning in the macaque posterior parietal cortex

ABSTRACTNeurons in the macaque posterior parietal cortex are known to encode the direction of self-motion. But do they also encode one’s speed? To test this, we performed neural recordings from area 7a while monkeys were passively translated or rotated at various speeds. Visual stimuli were delivered as optic flow fields and vestibular stimuli were generated by a motion platform. Under both conditions, the responses of a fraction of neurons scaled linearly with self-motion speed, and speed-selective neurons were not localized to specific layers or columns. We analyzed ensembles of simultaneously recorded neurons and found that the precision of speed representation was sufficient to support path integration over modest distances. Our findings describe a multisensory neural code for linear and angular self-motion speed in the posterior parietal cortex of the macaque brain, and suggest a potential role for this representation.

Top-down beta enhances bottom-up gamma

Several recent studies have demonstrated that the bottom-up signaling of a visual stimulus is subserved by interareal gamma-band synchronization, whereas top-down influences are mediated by alpha-beta band synchronization. These processes may implement top-down control of stimulus processing if top-down and bottom-up mediating rhythms are coupled via cross-frequency interaction. To test this possibility, we investigated Granger-causal influences among awake male macaque primary visual area V1, higher visual area V4 and parietal control area 7a during attentional task performance. Top-down 7a-to-V1 beta-band influences enhanced visually driven V1-to-V4 gamma-band influences. This enhancement was spatially specific and largest when beta-band activity preceded gamma-band activity by ∼0.1 s, suggesting a causal effect of top-down processes on bottom-up processes. We propose that this cross-frequency interaction mechanistically subserves the attentional control of stimulus selection.Significance StatementContemporary research indicates that the alpha-beta frequency band underlies top-down control, while the gamma-band mediates bottom-up stimulus processing. This arrangement inspires an attractive hypothesis, which posits that top-down beta-band influences directly modulate bottom-up gamma band influences via cross-frequency interaction. We evaluate this hypothesis determining that beta-band top-down influences from parietal area 7a to visual area V1 are correlated with bottom-up gamma frequency oscillations from V1 to area V4, in a spatially specific manner, and that this correlation is maximal when top-down activity precedes bottom-up activity. These results show that for top-down processes such as spatial attention, elevated top-down beta-band influences directly enhance feedforward stimulus induced gamma-band processing, leading to enhancement of the selected stimulus.

Spatial summation in macaque parietal area 7a follows a winner-take-all rule

While neurons in posterior parietal cortex have been found to signal the presence of a salient stimulus among multiple items in a display, spatial summation within their receptive field in the absence of an attentional bias has never been investigated. This information, however, is indispensable when one investigates the mechanisms of spatial attention and competition between multiple visual objects. To examine the spatial summation rule in parietal area 7a neurons, we trained rhesus monkeys to fixate on a central cross while two identical stimuli were briefly displayed in a neuron's receptive field. The response to a pair of dots was compared with the responses to the same dots when they were presented individually. The scaling and power parameters of a generalized summation algorithm varied greatly, both across neurons and across combinations of stimulus locations. However, the averaged response of the recorded population of 7a neurons was consistent with a winner-take-all rule for spatial summation. A control experiment where a monkey covertly attended to both stimuli simultaneously suggests that attention introduces additional competition by facilitating the less optimal stimulus. Thus an averaging stage is introduced between ∼200 and 300 ms of the response to a pair of stimuli. In short, the summation algorithm over the population of area 7a neurons carries the signature of a winner-take-all operation, with spatial attention possibly influencing the temporal dynamics of stimulus competition, that is the moment that the “winner” takes “victory” over the “loser” stimulus.

Neural Representation During Visually Guided Reaching in Macaque Posterior Parietal Cortex

Visually guided hand movements in primates require an interconnected network of various cortical areas. Single unit firing rate from area 7a and dorsal prelunate (DP) neurons of macaque posterior parietal cortex (PPC) was recorded during reaching movements to targets at variable locations and under different eye position conditions. In the eye position–varied task, the reach target was always foveated; thus eye position varied with reach target location. In the retinal-varied task, the monkey reached to targets at variable retinotopic locations while eye position was kept constant in the center. Spatial tuning was examined with respect to temporal (task epoch) and contextual (task condition) aspects, and response fields were compared. The analysis showed distinct tuning types. The majority of neurons changed their gain field tuning and retinotopic tuning between different phases of the task. Between the onset of visual stimulation and the preparatory phase (before the go signal), about one half the neurons altered their firing rate significantly. Spatial response fields during preparation and initiation epochs were strongly influenced by the task condition (eye position varied vs. retinal varied), supporting a strong role of eye position during visually guided reaching. DP neurons, classically considered visual, showed reach related modulation similar to 7a neurons. This study shows that both area 7a and DP are modulated during reaching behavior in primates. The various tuning types in both areas suggest distinct populations recruiting different circuits during visually guided reaching.