scholarly journals Signature patterns for top-down and bottom-up information processing via cross-frequency coupling in macaque auditory cortex

2018 ◽  
Author(s):  
Christian D. Márton ◽  
Makoto Fukushima ◽  
Corrie R. Camalier ◽  
Simon R. Schultz ◽  
Bruno B. Averbeck

AbstractPredictive coding is a theoretical framework that provides a functional interpretation of top-down and bottom up interactions in sensory processing. The theory has suggested that specific frequency bands relay bottom-up and top-down information (e.g. “γ up, β down”). But it remains unclear whether this notion generalizes to cross-frequency interactions. Furthermore, most of the evidence so far comes from visual pathways. Here we examined cross-frequency coupling across four sectors of the auditory hierarchy in the macaque. We computed two measures of cross-frequency coupling, phase-amplitude coupling (PAC) and amplitude-amplitude coupling (AAC). Our findings revealed distinct patterns for bottom-up and top-down information processing among cross-frequency interactions. Both top-down and bottom-up made prominent use of low frequencies: low-to-low frequency (θ, α, β) and low frequency-to-high γ couplings were predominant top-down, while low frequency-to-low γ couplings were predominant bottom-up. These patterns were largely preserved across coupling types (PAC and AAC) and across stimulus types (natural and synthetic auditory stimuli), suggesting they are a general feature of information processing in auditory cortex. Moreover, our findings showed that low-frequency PAC alternated between predominantly top-down or bottom-up over time. Altogether, this suggests sensory information need not be propagated along separate frequencies upwards and downwards. Rather, information can be unmixed by having low frequencies couple to distinct frequency ranges in the target region, and by alternating top-down and bottom-up processing over time.1SignificanceThe brain consists of highly interconnected cortical areas, yet the patterns in directional cortical communication are not fully understood, in particular with regards to interactions between different signal components across frequencies. We employed a a unified, computationally advantageous Granger-causal framework to examine bi-directional cross-frequency interactions across four sectors of the auditory cortical hierarchy in macaques. Our findings extend the view of cross-frequency interactions in auditory cortex, suggesting they also play a prominent role in top-down processing. Our findings also suggest information need not be propagated along separate channels up and down the cortical hierarchy, with important implications for theories of information processing in the brain such as predictive coding.

eNeuro ◽  
2019 ◽  
Vol 6 (2) ◽  
pp. ENEURO.0467-18.2019 ◽  
Author(s):  
Christian D. Márton ◽  
Makoto Fukushima ◽  
Corrie R. Camalier ◽  
Simon R. Schultz ◽  
Bruno B. Averbeck

2013 ◽  
Vol 25 (2) ◽  
pp. 175-187 ◽  
Author(s):  
Jihoon Oh ◽  
Jae Hyung Kwon ◽  
Po Song Yang ◽  
Jaeseung Jeong

Neural responses in early sensory areas are influenced by top–down processing. In the visual system, early visual areas have been shown to actively participate in top–down processing based on their topographical properties. Although it has been suggested that the auditory cortex is involved in top–down control, functional evidence of topographic modulation is still lacking. Here, we show that mental auditory imagery for familiar melodies induces significant activation in the frequency-responsive areas of the primary auditory cortex (PAC). This activation is related to the characteristics of the imagery: when subjects were asked to imagine high-frequency melodies, we observed increased activation in the high- versus low-frequency response area; when the subjects were asked to imagine low-frequency melodies, the opposite was observed. Furthermore, we found that A1 is more closely related to the observed frequency-related modulation than R in tonotopic subfields of the PAC. Our findings suggest that top–down processing in the auditory cortex relies on a mechanism similar to that used in the perception of external auditory stimuli, which is comparable to early visual systems.


2019 ◽  
Author(s):  
Yuru Song ◽  
Mingchen Yao ◽  
Helen Kemprecos ◽  
Áine Byrne ◽  
Zhengdong Xiao ◽  
...  

AbstractPain is a complex, multidimensional experience that involves dynamic interactions between sensory-discriminative and affective-emotional processes. Pain experiences have a high degree of variability depending on their context and prior anticipation. Viewing pain perception as a perceptual inference problem, we use a predictive coding paradigm to characterize both evoked and spontaneous pain. We record the local field potentials (LFPs) from the primary somatosensory cortex (S1) and the anterior cingulate cortex (ACC) of freely behaving rats—two regions known to encode the sensory-discriminative and affective-emotional aspects of pain, respectively. We further propose a framework of predictive coding to investigate the temporal coordination of oscillatory activity between the S1 and ACC. Specifically, we develop a high-level, empirical and phenomenological model to describe the macroscopic dynamics of bottom-up and top-down activity. Supported by recent experimental data, we also develop a mechanistic mean-field model to describe the mesoscopic population neuronal dynamics in the S1 and ACC populations, in both naive and chronic pain-treated animals. Our proposed predictive coding models not only replicate important experimental findings, but also provide new mechanistic insight into the uncertainty of expectation, placebo or nocebo effect, and chronic pain.Author SummaryPain perception in the mammalian brain is encoded through multiple brain circuits. The experience of pain is often associated with brain rhythms or neuronal oscillations at different frequencies. Understanding the temporal coordination of neural oscillatory activity from different brain regions is important for dissecting pain circuit mechanisms and revealing differences between distinct pain conditions. Predictive coding is a general computational framework to understand perceptual inference by integrating bottom-up sensory information and top-down expectation. Supported by experimental data, we propose a predictive coding framework for pain perception, and develop empirical and biologically-constrained computational models to characterize oscillatory dynamics of neuronal populations from two cortical circuits—one for the sensory-discriminative experience and the other for affective-emotional experience, and further characterize their temporal coordination under various pain conditions. Our computational study of biologically-constrained neuronal population model reveals important mechanistic insight on pain perception, placebo analgesia, and chronic pain.


2015 ◽  
Vol 112 (43) ◽  
pp. 13401-13406 ◽  
Author(s):  
Christoph Teufel ◽  
Naresh Subramaniam ◽  
Veronika Dobler ◽  
Jesus Perez ◽  
Johanna Finnemann ◽  
...  

Many neuropsychiatric illnesses are associated with psychosis, i.e., hallucinations (perceptions in the absence of causative stimuli) and delusions (irrational, often bizarre beliefs). Current models of brain function view perception as a combination of two distinct sources of information: bottom-up sensory input and top-down influences from prior knowledge. This framework may explain hallucinations and delusions. Here, we characterized the balance between visual bottom-up and top-down processing in people with early psychosis (study 1) and in psychosis-prone, healthy individuals (study 2) to elucidate the mechanisms that might contribute to the emergence of psychotic experiences. Through a specialized mental-health service, we identified unmedicated individuals who experience early psychotic symptoms but fall below the threshold for a categorical diagnosis. We observed that, in early psychosis, there was a shift in information processing favoring prior knowledge over incoming sensory evidence. In the complementary study, we capitalized on subtle variations in perception and belief in the general population that exhibit graded similarity with psychotic experiences (schizotypy). We observed that the degree of psychosis proneness in healthy individuals, and, specifically, the presence of subtle perceptual alterations, is also associated with stronger reliance on prior knowledge. Although, in the current experimental studies, this shift conferred a performance benefit, under most natural viewing situations, it may provoke anomalous perceptual experiences. Overall, we show that early psychosis and psychosis proneness both entail a basic shift in visual information processing, favoring prior knowledge over incoming sensory evidence. The studies provide complementary insights to a mechanism by which psychotic symptoms may emerge.


Author(s):  
Mariana von Mohr ◽  
Aikaterini Fotopoulou

Pain and pleasant touch have been recently classified as interoceptive modalities. This reclassification lies at the heart of long-standing debates questioning whether these modalities should be defined as sensations on their basis of neurophysiological specificity at the periphery or as homeostatic emotions on the basis of top-down convergence and modulation at the spinal and brain levels. Here, we outline the literature on the peripheral and central neurophysiology of pain and pleasant touch. We next recast this literature within a recent Bayesian predictive coding framework, namely active inference. This recasting puts forward a unifying model of bottom-up and top-down determinants of pain and pleasant touch and the role of social factors in modulating the salience of peripheral signals reaching the brain.


2018 ◽  
Author(s):  
Hyojin Park ◽  
Gregor Thut ◽  
Joachim Gross

AbstractNatural communication between interlocutors is enabled by the ability to predict upcoming speech in a given context. Previously we showed that these predictions rely on a fronto-motor top-down control of low-frequency oscillations in auditory-temporal brain areas that track intelligible speech. However, a comprehensive spatio-temporal characterisation of this effect is still missing. Here, we applied transfer entropy to source-localised MEG data during continuous speech perception. First, at low frequencies (1-4 Hz, brain delta phase to speech delta phase), predictive effects start in left fronto-motor regions and progress to right temporal regions. Second, at higher frequencies (14-18 Hz, brain beta power to speech delta phase), predictive patterns show a transition from left inferior frontal gyrus via left precentral gyrus to left primary auditory areas. Our results suggest a progression of prediction processes from higher-order to early sensory areas in at least two different frequency channels.


Perception ◽  
1993 ◽  
Vol 22 (5) ◽  
pp. 517-526 ◽  
Author(s):  
Okihide Hikosaka ◽  
Satoru Miyauchi ◽  
Shinsuke Shimojo

Attention may be drawn passively to a visually salient object. We may also actively direct attention to an object of interest. Do the two kinds of attention, passive and active, interact and jointly influence visual information processing at some neural level? What happens if the passive and active attentions come into conflict? These questions were addressed with the aid of a novel psychophysical technique which reveals an attentional gradient as a sensation of motion in a line which is presented instantaneously. The subjects were asked to direct attention with voluntary effort: to the side opposite to a stimulus change, to an object with a predetermined colour, and to an object moving smoothly. In every case the same motion sensation was induced in the line from the attended side to the unattended side. This voluntary attention, however, can easily and quickly be distracted by a change in the periphery, though it can be regained within a period of 200 to 500 ms. The results suggest that the line motion can be induced in voluntary (top-down) as well as stimulus-driven (bottom-up) situations, thus indicating the truly attentional nature of the effect, rather than it being some kind of retinotopic sensory artifact or response bias. The results also suggest that these two kinds of attention have facilitatory effects acting together on a relatively early stage of visual information processing.


1995 ◽  
Vol 80 (2) ◽  
pp. 447-465 ◽  
Author(s):  
Elizabeth K. Dreben ◽  
John H. Fryer ◽  
Douglas M. McNair

Schizophrenic patients ( n = 20), depressive patients ( n = 20), and normal adults ( n = 20) were compared on global vs local analyses of perceptual information using tachistoscopic tasks and on top-down vs bottom-up conceptual processing using card-sort tasks. The schizophrenic group performed more poorly on tasks requiring either global analyses (counting lines when distracting circles were present) or top-down conceptual processing (rule learning) than they did on tasks requiring local analyses (counting heterogeneous lines) or bottom-up processing (attribute identification). The schizophrenic group appeared not to use conceptually guided processing. Normal adults showed the reverse pattern. The depressive group performed similarly to the schizophrenic group on perceptual tasks but closer to the normal group on conceptual tasks, thereby appearing to be less dependent on a particular information-processing strategy. These deficits in organizational strategy may be related to the use of available processing resources as well as the allocation of attention.


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