Processing In Sensory Cortex Research Articles

Behavioral decomposition reveals rich encoding structure employed across neocortex in rats

The cortical population code is pervaded by activity patterns evoked by movement, but it remains largely unknown how such signals relate to natural behavior or how they might support processing in sensory cortices where they have been observed. To address this we compared high-density neural recordings across four cortical regions (visual, auditory, somatosensory, motor) in relation to sensory modulation, posture, movement, and ethograms of freely foraging male rats. Momentary actions, such as rearing or turning, were represented ubiquitously and could be decoded from all sampled structures. However, more elementary and continuous features, such as pose and movement, followed region-specific organization, with neurons in visual and auditory cortices preferentially encoding mutually distinct head-orienting features in world-referenced coordinates, and somatosensory and motor cortices principally encoding the trunk and head in egocentric coordinates. The tuning properties of synaptically coupled cells also exhibited connection patterns suggestive of area-specific uses of pose and movement signals, particularly in visual and auditory regions. Together, our results indicate that ongoing behavior is encoded at multiple levels throughout the dorsal cortex, and that low-level features are differentially utilized by different regions to serve locally relevant computations.

Excitatory Crossmodal Input to a Widespread Population of Primary Sensory Cortical Neurons.

Crossmodal information processing in sensory cortices has been reported in sparsely distributed neurons under normal conditions and can undergo experience- or activity-induced plasticity. Given the potential role in brain function as indicated by previous reports, crossmodal connectivity in the sensory cortex needs to be further explored. Using perforated whole-cell recording in anesthetized adult rats, we found that almost all neurons recorded in the primary somatosensory, auditory, and visual cortices exhibited significant membrane-potential responses to crossmodal stimulation, as recorded when brain activity states were pharmacologically down-regulated in light anesthesia. These crossmodal cortical responses were excitatory and subthreshold, and further seemed to be relayed primarily by the sensory thalamus, but not the sensory cortex, of the stimulated modality. Our experiments indicate a sensory cortical presence of widespread excitatory crossmodal inputs, which might play roles in brain functions involving crossmodal information processing or plasticity.

Simultaneous mapping of neural activities in auditory and visual cortex of rat

AbstractIn the mammalian cerebral cortex, each sensory cortex plays a central role in the information processing of each sensory modality, yet the cross‐modal interactions between sensory cortices remains to be elucidated. Herein, we designed a surface electrode array with 32 recording sites and established a novel electrophysiological technique to record neural activities simultaneously from the auditory and visual cortices of anesthetized rats. We evaluated our mapping in two ways; first, the middle‐latency potentials in the auditory‐evoked potentials and visual‐evoked potentials were localized in the auditory and visual cortex, respectively. Second, the microelectrode array successfully recorded auditory and visual mismatch negativity (aMMN and vMMN), which is one of the neural activities reported to reflect cross‐modal interactions in previous human studies. In addition, we demonstrated that MMN distributed beyond the border between these sensory cortices, suggesting cross‐modal interactions between these areas. Taken together, the present recording technique will contribute to elucidating cross‐modality information processing in sensory cortices.

Multisensory-Guided Associative Learning Enhances Multisensory Representation in Primary Auditory Cortex.

Sensory cortices, classically considered to represent modality-specific sensory information, are also found to engage in multisensory processing. However, how sensory processing in sensory cortices is cross-modally modulated remains an open question. Specifically, we understand little of cross-modal representation in sensory cortices in perceptual tasks and how perceptual learning modifies this process. Here, we recorded neural responses in primary auditory cortex (A1) both while freely moving rats discriminated stimuli in Go/No-Go tasks and when anesthetized. Our data show that cross-modal representation in auditory cortices varies with task contexts. In the task of an audiovisual cue being the target associating with water reward, a significantly higher proportion of auditory neurons showed a visually evoked response. The vast majority of auditory neurons, if processing auditory-visual interactions, exhibit significant multisensory enhancement. However, when the rats performed tasks with unisensory cues being the target, cross-modal inhibition, rather than enhancement, predominated. In addition, multisensory associational learning appeared to leave a trace of plastic change in A1, as a larger proportion of A1 neurons showed multisensory enhancement in anesthesia. These findings indicate that multisensory processing in principle sensory cortices is not static, and having cross-modal interaction in the task requirement can substantially enhance multisensory processing in sensory cortices.

Movement and VIP Interneuron Activation Differentially Modulate Encoding in Mouse Auditory Cortex.

Information processing in sensory cortex is highly sensitive to nonsensory variables such as anesthetic state, arousal, and task engagement. Recent work in mouse visual cortex suggests that evoked firing rates, stimulus-response mutual information, and encoding efficiency increase when animals are engaged in movement. A disinhibitory circuit appears central to this change: inhibitory neurons expressing vasoactive intestinal peptide (VIP) are activated during movement and disinhibit pyramidal cells by suppressing other inhibitory interneurons. Paradoxically, although movement activates a similar disinhibitory circuit in auditory cortex (ACtx), most ACtx studies report reduced spiking during movement. It is unclear whether the resulting changes in spike rates result in corresponding changes in stimulus-response mutual information. We examined ACtx responses evoked by tone cloud stimuli, in awake mice of both sexes, during spontaneous movement and still conditions. VIP+ cells were optogenetically activated on half of trials, permitting independent analysis of the consequences of movement and VIP activation, as well as their intersection. Movement decreased stimulus-related spike rates as well as mutual information and encoding efficiency. VIP interneuron activation tended to increase stimulus-evoked spike rates but not stimulus-response mutual information, thus reducing encoding efficiency. The intersection of movement and VIP activation was largely consistent with a linear combination of these main effects: VIP activation recovered movement-induced reduction in spike rates, but not information transfer.

A Sensorimotor Pathway via Higher-Order Thalamus.

We now know that sensory processing in cortex occurs not only via direct communication between primary to secondary areas, but also via their parallel cortico-thalamo-cortical (i.e., trans-thalamic) pathways. Both corticocortical and trans-thalamic pathways mainly signal through glutamatergic class 1 (driver) synapses, which have robust and efficient synaptic dynamics suited for the transfer of information such as receptive field properties, suggesting the importance of class 1 synapses in feedforward, hierarchical processing. However, such a parallel arrangement has only been identified in sensory cortical areas: visual, somatosensory, and auditory. To test the generality of trans-thalamic pathways, we sought to establish its presence beyond purely sensory cortices to determine whether there is a trans-thalamic pathway parallel to the established primary somatosensory (S1) to primary motor (M1) pathway. We used trans-synaptic viral tracing, optogenetics in slice preparations, and bouton size analysis in the mouse (both sexes) to document that a circuit exists from layer 5 of S1 through the posterior medial nucleus of the thalamus to M1 with glutamatergic class 1 properties. This represents a hitherto unknown, robust sensorimotor linkage and suggests that the arrangement of parallel direct and trans-thalamic corticocortical circuits may be present as a general feature of cortical functioning.SIGNIFICANCE STATEMENT During sensory processing, feedforward pathways carry information such as receptive field properties via glutamatergic class 1 synapses, which have robust and efficient synaptic dynamics. As expected, class 1 synapses subserve the feedforward projection from primary to secondary sensory cortex, but also a route through specific higher-order thalamic nuclei, creating a parallel feedforward trans-thalamic pathway. We now extend the concept of cortical areas being connected via parallel, direct, and trans-thalamic circuits from purely sensory cortices to a sensorimotor cortical circuit (i.e., primary sensory cortex to primary motor cortex). This suggests a generalized arrangement for corticocortical communication.

A learning rule that explains how rewards teach attention

Many theories propose that top-down attentional signals control processing in sensory cortices by modulating neural activity. But who controls the controller? Here we investigate how a biologically plausible neural reinforcement learning scheme can create higher order representations and top-down attentional signals. The learning scheme trains neural networks using two factors that gate Hebbian plasticity: (1) an attentional feedback signal from the response-selection stage to earlier processing levels; and (2) a globally available neuromodulator that encodes the reward prediction error. We demonstrate how the neural network learns to direct attention to one of two coloured stimuli that are arranged in a rank-order. Like monkeys trained on this task, the network develops units that are tuned to the rank-order of the colours and it generalizes this newly learned rule to previously unseen colour combinations. These results provide new insight into how individuals can learn to control attention as a function of reward contingency.

Ventral tegmental area activation promotes firing precision and strength through circuit inhibition in the primary auditory cortex.

The activation of the ventral tegmental area (VTA) can rebuild the tonotopic representation in the primary auditory cortex (A1), but the cellular mechanisms remain largely unknown. Here, we investigated the firing patterns and membrane potential dynamics of neurons in A1 under the influence of VTA activation using in vivo intracellular recording. We found that VTA activation can significantly reduce the variability of sound evoked responses and promote the firing precision and strength of A1 neurons. Furthermore, the compressed response window was caused by an early hyperpolarization as a result of enhanced circuit inhibition. Our study suggested a possible mechanism of how the reward system affects information processing in sensory cortex: VTA activation strengthens cortical inhibition, which shortens the response window of post-synaptic cortical neurons and further promotes the precision and strength of neuronal activity.

Flexibility and Stability in Sensory Processing Revealed Using Visual-to-Auditory Sensory Substitution

The classical view of sensory processing involves independent processing in sensory cortices and multisensory integration in associative areas. This hierarchical structure has been challenged by evidence of multisensory responses in sensory areas, and dynamic weighting of sensory inputs in associative areas, thus far reported independently. Here, we used a visual-to-auditory sensory substitution algorithm (SSA) to manipulate the information conveyed by sensory inputs while keeping the stimuli intact. During scan sessions before and after SSA learning, subjects were presented with visual images and auditory soundscapes. The findings reveal 2 dynamic processes. First, crossmodal attenuation of sensory cortices changed direction after SSA learning from visual attenuations of the auditory cortex to auditory attenuations of the visual cortex. Secondly, associative areas changed their sensory response profile from strongest response for visual to that for auditory. The interaction between these phenomena may play an important role in multisensory processing. Consistent features were also found in the sensory dominance in sensory areas and audiovisual convergence in associative area Middle Temporal Gyrus. These 2 factors allow for both stability and a fast, dynamic tuning of the system when required.

A disinhibitory circuit mediates motor integration in the somatosensory cortex.

The influence of motor activity on sensory processing is crucial for perception and motor execution. However, the underlying circuits are not known. To unravel the circuit by which activity in the primary vibrissal motor cortex (vM1) modulates sensory processing in the primary somatosensory barrel cortex (S1), we used optogenetics to examine the long-range inputs from vM1 to the various neuronal elements in S1. We found that S1-projecting vM1 pyramidal neurons strongly recruited vasointestinal peptide (VIP)-expressing GABAergic interneurons, a subset of serotonin receptor-expressing interneurons. These VIP interneurons preferentially inhibited somatostatin-expressing interneurons, neurons that target the distal dendrites of pyramidal cells. Consistent with this vM1-mediated disinhibitory circuit, the activity of VIP interneurons in vivo increased and that of somatostatin interneurons decreased during whisking. These changes in firing rates during whisking depended on vM1 activity. Our results suggest previously unknown circuitry by which inputs from motor cortex influence sensory processing in sensory cortex.

Getting a handle on how the brain generates complexity

Sensory processing in cortex across modalities appears to rely on a “simple-to-complex” hierarchical computational strategy in which neurons at later levels in the hierarchy combine inputs from earlier levels to create more complex neuronal selectivities. The specifics of this process are still poorly understood, however. In this issue of Network, Plebe shows how computational modeling of experimental data on neuronal tuning in secondary visual cortex can help us understand how the brain increases neuronal tuning complexity across the visual cortical hierarchy.

The role of the pulvinar in resolving competition between memory and visual selection: A functional connectivity study

Memory and attention interact. Information held in working memory (WM) can bias visual selection toward matching stimuli in a subsequent search display, while a search target that is different from the memory stimulus can interfere with its subsequent recognition. In recent fMRI studies, the pulvinar has been consistently shown to have an enhanced response when an item in WM matches a search target and a reduced response when the WM item matches a distracter in search. Here we used Granger causality analysis to help understand the role of the pulvinar in resolving competition between memory and selection processes. Across three experiments the results showed increased coupling between the pulvinar and the ipsilateral superior frontal gyrus, contralateral temporal–parietal junction (TPJ) and calcarine sulcus when a visual search distracter matched the item held in memory. This connection pattern suggests that the pulvinar suppresses visual responses to the target when a contralateral distracter contains information held in working memory. We propose that this suppression acts to protect the memory item from interference arising from information associated with the search target. Consistent with this proposal we showed that the strength of the thalamus-to-visual connection predicted performance on a subsequent memory test. The data therefore suggest that the thalamus modulates bottom up processing in sensory cortex to minimize interference to WM content.

Spike-Phase Coding Boosts and Stabilizes Information Carried by Spatial and Temporal Spike Patterns

Several neural codes have been proposed in order to explain how neurons encode sensory information. Here we tested the hypothesis that different codes might be employed concurrently and provide complementary stimulus information. Quantifying the information encoded about natural sounds in the auditory cortex of alert animals, we found that temporal spike-train patterns and spatial populations were both highly informative. However, the relative phase of slow ongoing rhythms at which these (temporal or population) responses occurred provided much additional and complementary information. Such nested codes combining spike-train patterns with the phase of firing were not only most informative, but also most robust to sensory noise added to the stimulus. Our findings suggest that processing in sensory cortices could rely on the concurrent use of several codes that combine information across different spatiotemporal scales. In addition, they propose a role of slow cortical rhythms in stabilizing sensory representations by reducing effects of noise.

The neural circuitry underlying the executive control of auditory spatial attention

Although a fronto-parietal network has consistently been implicated in the control of visual spatial attention, the network that guides spatial attention in the auditory domain is not yet clearly understood. To investigate this issue, we measured brain activity using functional magnetic resonance imaging while participants performed a cued auditory spatial attention task. We found that cued orienting of auditory spatial attention activated a medial–superior distributed fronto-parietal network. In addition, we found cue-triggered increases of activity in the auditory sensory cortex prior to the occurrence of an auditory target, suggesting that auditory attentional control operates in part by biasing processing in sensory cortex in favor of expected target stimuli. Finally, an exploratory cross-study comparison further indicated several common frontal and parietal regions as being involved in the control of both visual and auditory spatial attention. Thus, the present findings not only reveal the network of brain areas underlying endogenous spatial orienting in the auditory modality, but also suggest that the control of spatial attention in different sensory modalities is enabled in part by some common, supramodal neural mechanisms.

The Missing Piece in the "Use It or Lose It" Puzzle: Is Inhibition Regulated by Activity or Does it Act on its Own Accord?

We have gained enormous insight into the mechanisms underlying both activity-dependent and (to a lesser degree) -independent plasticity of excitatory synapses. Recently, cortical inhibition has been shown to play a vital role in the formation of critical periods for sensory plasticity. As such, sculpting of neuronal circuits by inhibition may be a common mechanism by which activity organizes or reorganizes brain circuits. Disturbances in the balance of excitation and inhibition in the neocortex provoke abnormal activities, such as epileptic seizures and abnormal cortical development. However, both the process of experience-dependent postnatal maturation of neocortical inhibitory networks and its underlying mechanisms remain elusive. Mechanisms that match excitation and inhibition are central to achieving balanced function at the level of individual circuits. The goal of this review is to reinforce our understanding of the mechanisms by which developing inhibitory networks are able to adapt to sensory inputs, and to maintain their balance with developing excitatory networks. Discussion is centered on the following questions related to experience-dependent plasticity of neocortical inhibitory networks: 1) What are the roles of GABAergic inhibition in the postnatal maturation of neocortical circuits? 2) Does the maturation of neocortical inhibitory circuits proceed in an activity-dependent manner or do they develop independently of sensory inputs? 3) Does activity regulate inhibitory networks in the same way it regulates excitatory networks? 4) What are the molecular and cellular mechanisms that underlie the activity-dependent maturation of inhibitory networks? 5) What are the functional advantages of experience-dependent plasticity of inhibitory networks to network processing in sensory cortices?

Toward an Explanation of the Genesis of Ketamine-Induced Perceptual Distortions and Hallucinatory States

The NMDA receptor (NMDAR) channel has been proposed to function as a coincidence-detection mechanism for afferent and reentrant signals, supporting conscious perception, learning, and memory formation. In this paper we discuss the genesis of distorted perceptual states induced by subanesthetic doses of ketamine, a well-known NMDA antagonist. NMDAR blockage has been suggested to perturb perceptual processing in sensory cortex, and also to decrease GABAergic inhibition in limbic areas (leading to an increase in dopamine excitability). We propose that perceptual distortions and hallucinations induced by ketamine blocking of NMDARs are generated by alternative signaling pathways, which include increase of excitability in frontal areas, and glutamate binding to AMPA in sensory cortex prompting Ca CC entry through voltage-dependent calcium channels (VDCCs). This mechanism supports the thesis that glutamate binding to AMPA and NMDARs at sensory cortex mediates most normal perception, while binding to AMPA and activating VDCCs mediates some types of altered perceptual states. We suggest that Ca CC metabolic activity in neurons at associative and sensory cortices is an important factor in the generation of both kinds of perceptual consciousness.