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A Diversity of Intrinsic Timescales Underlie Neural Computations.
Neural processing occurs across a range of temporal scales. To facilitate this, the brain uses fast-changing representations reflecting momentary sensory input alongside more temporally extended representations, which integrate across both short and long temporal windows. The temporal flexibility of these representations allows animals to behave adaptively. Short temporal windows facilitate adaptive responding in dynamic environments, while longer temporal windows promote the gradual integration of information across time. In the cognitive and motor domains, the brain sets overarching goals to be achieved within a long temporal window, which must be broken down into sequences of actions and precise movement control processed across much shorter temporal windows. Previous human neuroimaging studies and large-scale artificial network models have ascribed different processing timescales to different cortical regions, linking this to each region's position in an anatomical hierarchy determined by patterns of inter-regional connectivity. However, even within cortical regions, there is variability in responses when studied with single-neuron electrophysiology. Here, we review a series of recent electrophysiology experiments that demonstrate the heterogeneity of temporal receptive fields at the level of single neurons within a cortical region. This heterogeneity appears functionally relevant for the computations that neurons perform during decision-making and working memory. We consider anatomical and biophysical mechanisms that may give rise to a heterogeneity of timescales, including recurrent connectivity, cortical layer distribution, and neurotransmitter receptor expression. Finally, we reflect on the computational relevance of each brain region possessing a heterogeneity of neuronal timescales. We argue that this architecture is of particular importance for sensory, motor, and cognitive computations.
The promise of layer-specific neuroimaging for testing predictive coding theories of psychosis.
Predictive coding potentially provides an explanatory model for understanding the neurocognitive mechanisms of psychosis. It proposes that cognitive processes, such as perception and inference, are implemented by a hierarchical system, with the influence of each level being a function of the estimated precision of beliefs at that level. However, predictive coding models of psychosis are insufficiently constrained-any phenomenon can be explained in multiple ways by postulating different changes to precision at different levels of processing. One reason for the lack of constraint in these models is that the core processes are thought to be implemented by the function of specific cortical layers, and the technology to measure layer specific neural activity in humans has until recently been lacking. As a result, our ability to constrain the models with empirical data has been limited. In this review we provide a brief overview of predictive processing models of psychosis and then describe the potential for newly developed, layer specific neuroimaging techniques to test and thus constrain these models. We conclude by discussing the most promising avenues for this research as well as the technical and conceptual challenges which may limit its application.
Incidence of neurodegenerative and cerebrovascular diseases associated with antihypertensive drug classes.
Antihypertensive drugs (AHTs) are associated with lowered risks of neurodegenerative diseases and stroke. However, the relative risks associated with different AHT classes are unclear. Using an electronic health record network with 34 million eligible patients, we compared rates of these disorders over a 2-year period, in propensity score-matched cohorts of people taking calcium channel blockers (CCBs) compared with those taking other AHT classes. CCBs were associated with a higher incidence of all disorders compared with renin-angiotensin system agents, and a higher incidence of dementia and cerebrovascular disease compared with diuretics. CCBs were associated with a lower incidence of movement disorders and cerebrovascular disease compared with beta-blockers. The data show that AHT classes confer differential risks of neurodegenerative and cerebrovascular diagnoses.
Time in Cortical Circuits.
UNLABELLED: Time is central to cognition. However, the neural basis for time-dependent cognition remains poorly understood. We explore how the temporal features of neural activity in cortical circuits and their capacity for plasticity can contribute to time-dependent cognition over short time scales. This neural activity is linked to cognition that operates in the present or anticipates events or stimuli in the near future. We focus on deliberation and planning in the context of decision making as a cognitive process that integrates information across time. We progress to consider how temporal expectations of the future modulate perception. We propose that understanding the neural basis for how the brain tells time and operates in time will be necessary to develop general models of cognition. SIGNIFICANCE STATEMENT: Time is central to cognition. However, the neural basis for time-dependent cognition remains poorly understood. We explore how the temporal features of neural activity in cortical circuits and their capacity for plasticity can contribute to time-dependent cognition over short time scales. We propose that understanding the neural basis for how the brain tells time and operates in time will be necessary to develop general models of cognition.
The Cumulative Effects of Predictability on Synaptic Gain in the Auditory Processing Stream.
Stimulus predictability can lead to substantial modulations of brain activity, such as shifts in sustained magnetic field amplitude, measured with magnetoencephalography (MEG). Here, we provide a mechanistic explanation of these effects using MEG data acquired from healthy human volunteers (N = 13, 7 female). In a source-level analysis of induced responses, we established the effects of orthogonal predictability manipulations of rapid tone-pip sequences (namely, sequence regularity and alphabet size) along the auditory processing stream. In auditory cortex, regular sequences with smaller alphabets induced greater gamma activity. Furthermore, sequence regularity shifted induced activity in frontal regions toward higher frequencies. To model these effects in terms of the underlying neurophysiology, we used dynamic causal modeling for cross-spectral density and estimated slow fluctuations in neural (postsynaptic) gain. Using the model-based parameters, we accurately explain the sensor-level sustained field amplitude, demonstrating that slow changes in synaptic efficacy, combined with sustained sensory input, can result in profound and sustained effects on neural responses to predictable sensory streams.SIGNIFICANCE STATEMENT Brain activity can be strongly modulated by the predictability of stimuli it is currently processing. An example of such a modulation is a shift in sustained magnetic field amplitude, measured with magnetoencephalography. Here, we provide a mechanistic explanation of these effects. First, we establish the oscillatory neural correlates of independent predictability manipulations in hierarchically distinct areas of the auditory processing stream. Next, we use a biophysically realistic computational model to explain these effects in terms of the underlying neurophysiology. Finally, using the model-based parameters describing neural gain modulation, we can explain the previously unexplained effects observed at the sensor level. This demonstrates that slow modulations of synaptic gain can result in profound and sustained effects on neural activity.
Competitive interactions affect working memory performance for both simultaneous and sequential stimulus presentation.
Competition between simultaneously presented visual stimuli lengthens reaction time and reduces both the BOLD response and neural firing. In contrast, conditions of sequential presentation have been assumed to be free from competition. Here we manipulated the spatial proximity of stimuli (Near versus Far conditions) to examine the effects of simultaneous and sequential competition on different measures of working memory (WM) for colour. With simultaneous presentation, the measure of WM precision was significantly lower for Near items, and participants reported the colour of the wrong item more often. These effects were preserved when the second stimulus immediately followed the first, disappeared when they were separated by 500 ms, and were partly recovered (evident for our measure of mis-binding but not WM precision) when the task was altered to encourage participants to maintain the sequentially presented items together in WM. Our results show, for the first time, that competition affects the measure of WM precision, and challenge the assumption that sequential presentation removes competition.
Temporal Anticipation Based on Memory.
The fundamental role that our long-term memories play in guiding perception is increasingly recognized, but the functional and neural mechanisms are just beginning to be explored. Although experimental approaches are being developed to investigate the influence of long-term memories on perception, these remain mostly static and neglect their temporal and dynamic nature. Here, we show that our long-term memories can guide attention proactively and dynamically based on learned temporal associations. Across two experiments, we found that detection and discrimination of targets appearing within previously learned contexts are enhanced when the timing of target appearance matches the learned temporal contingency. Neural markers of temporal preparation revealed that the learned temporal associations trigger specific temporal predictions. Our findings emphasize the ecological role that memories play in predicting and preparing perception of anticipated events, calling for revision of the usual conceptualization of contextual associative memory as a reflective and retroactive function.
Changing interpretations of emotional expressions in working memory with aging.
[Correction Notice: An Erratum for this article was reported online in Emotion on Jun 24 2019 (see record 2019-34942-001). In the article, the plots for Figure 3a shifted incorrectly to the right. The error bars should be centered on 10, 30, 50, 70, and 90. The corrected figure is present in the erratum.] Working memory (WM) shows significant decline with age. It is interesting to note that some research has suggested age-related impairments can be reduced in tasks that involve emotion-laden stimuli. However, only a few studies have explored how WM for emotional material changes in aging. Here we developed a novel experimental task to compare and contrast how emotional material is represented in older versus younger adults. The task enabled us to separate overall WM accuracy from emotional biases in the content of affective representations in WM. We found that, in addition to overall decline in WM performance, older adults showed a systematic positivity bias in representing information in WM relative to younger adults (positivity effect). They remembered fearful faces as being less fearful than younger adults and interpreted ambiguous facial expressions more positively. The findings show that aging brings a type of positivity bias when picking up affective information for guiding future behavior. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
Attention modulates maintenance of representations in visual short-term memory.
Recent studies have shown that selective attention is of considerable importance for encoding task-relevant items into visual short-term memory (VSTM) according to our behavioral goals. However, it is not known whether top-down attentional biases can continue to operate during the maintenance period of VSTM. We used ERPs to investigate this question across two experiments. Specifically, we tested whether orienting attention to a given spatial location within a VSTM representation resulted in modulation of the contralateral delay activity (CDA), a lateralized ERP marker of VSTM maintenance generated when participants selectively encode memory items from one hemifield. In both experiments, retrospective cues during the maintenance period could predict a specific item (spatial retrocue) or multiple items (neutral retrocue) that would be probed at the end of the memory delay. Our results revealed that VSTM performance is significantly improved by orienting attention to the location of a task-relevant item. The behavioral benefit was accompanied by modulation of neural activity involved in VSTM maintenance. Spatial retrocues reduced the magnitude of the CDA, consistent with a reduction in memory load. Our results provide direct evidence that top-down control modulates neural activity associated with maintenance in VSTM, biasing competition in favor of the task-relevant information.
Dissociable top-down anticipatory neural states for different linguistic dimensions.
When preparing to perform a task, the brain settles into task-set states which are relevant for the selection of the appropriate task-rules and stimulus-response mappings. The way this selection takes place within the Language domain is not well understood. We used high-density electrophysiological recordings while participants were engaged in a task in which cues directed their attention to the orthography, phonology or semantics of upcoming target words (or to the shape of novel symbols). To study the specificity of the brain preparatory states to different goals within the language domain, we contrasted the topographical maps associated with the cues for these different tasks, and explored whether the need of task-set reconfiguration modulated this preparatory activity. As a complement to the topographical analyses, we compared the amplitude of the cue-locked ERPs across task conditions. The topographical maps differed only at the end of the epoch. During this time window, each task-cue generated distinct topographical activity, which was also different depending on whether it involved a switch in task-set or not. These results suggest that, when the time of target onset approaches, the generators of anticipatory-biasing brain states for different language tasks vary depending on the nature of the task.
Orienting attention to instants in time.
My colleagues and I have investigated whether the temporal framework can be used to guide selective attention, and have applied non-invasive methodology to reveal the brain systems and mechanisms involved. Our findings show that we are able to orient attention selectively to different points in time, enhancing behavioral performance. These effects are mediated by a left-hemisphere dominant parietal-frontal system, which partially overlaps with the networks involved in spatial orienting. The neural system for temporal orienting also includes brain areas associated with motor preparation and anticipation, suggesting that sensorimotor areas with different specializations can contribute to attentional orienting depending on the stimulus attributes guiding selection. The optimization of behavior by temporal orienting involves enhancement of the latency and amplitude of event-related potentials that are associated with motor responses and decisions. The effects are distinct from those during visual spatial attention, indicating that behavioral advantages can be conferred by multiple types of neural mechanisms. Taken together, the findings illustrate the flexibility of attentional functions in the human brain.
Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts.
Temporal orienting of attention is the ability to focus resources at a particular moment in time in order to optimise behaviour, and is associated with activation of left parietal and premotor cortex [Coull, J. T., Nobre, A. C. Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. Journal of Neuroscience, 1998, 18, 7426-7435]. In the present experiment, we explored the behavioural and anatomical correlates of temporal orienting to foveal visual stimuli, in order to eliminate any spatial attention confounds. We implemented a two-way factorial design in an event-related fMRI study to examine the factors of trial validity (predictability of target by cue), length of delay (cue-target interval), and their interaction. There were two distinct types of invalid trial: those where attention was automatically drawn to a premature target and those where attention was voluntarily shifted to a delayed time-point. Reaction times for valid trials were shorter than those for invalid trials, demonstrating appropriate allocation of attention to temporal cues. All trial-types activated a shared system, including frontoparietal areas bilaterally, showing that this network is consistently associated with attentional orienting and is not specific to spatial tasks. Distinct brain areas were sensitive to cue-target delays and to trial validity. Long cue-target intervals activated areas involved in motor preparation: supplementary motor cortex, basal ganglia and thalamus. Invalid trials, where temporal expectancies were breached, showed enhanced activation of left parietal and frontal areas, and engagement of orbitofrontal cortex bilaterally. Finally, trial validity interacted with length of delay. Appearance of targets prematurely selectively activated visual extrastriate cortex; while postponement of target appearance selectively activated right prefrontal cortex. These findings suggest that distinct brain areas are involved in redirecting attention based upon sensory events (bottom-up, exogenous shifts) and based upon cognitive expectations (top-down, endogenous shifts).
The dynamics of shifting visuospatial attention revealed by event-related potentials.
We developed a behavioral task for spatial orienting of attention in which the same physical stimulus cued covert peripheral shifts of attention to either the left or the right visual fields in different conditions. The design enabled us to record the brain activity engaged during spatial shifts of covert attention that was independent from the physical characteristics of the cueing stimulus using event-related potentials (ERPs). ERPs elicited by foveal cues differed according to the predicted target location starting ca. 160 ms, and differences persisted until the occurrence of the target stimuli. Multiple processes were linked to shifting spatial attention during the cue-target interval. The earliest effects consisted of enhanced negative potentials over the posterior scalp contralateral to the cued location. Later effects were concentrated over the right anterior scalp sites, where activity associated with shifts to the right visual field elicited larger positive potentials. The results extend our understanding of the neural system that orients spatial attention by providing valuable information about the temporal dynamics and hemispheric asymmetries of activity within its posterior and anterior regions.
Language-Related ERPs: Scalp Distributions and Modulation by Word Type and Semantic Priming.
Abstract Event-related potentials (ERPs) were recorded from the scalp to investigate the processing of word stimuli. Three tasks were used: (1) a task comparing words that provided an anomalous or normal sentence ending, (2) a word-list task in which different word types were examined, and (3) a word-list task in which semantic priming was examined. ERPs were recorded from a 50-channel montage in an attempt to dissociate overlapping ERP features by their scalp distributions. The focus of these studies was the N400, an ERP previously associated with language processing (Kutas & Hillyard, 1980). The temporal interval typically associated with N400 (250-500 msec) was found to contain overlapping ERP features. Two of these features were common to both sentence and word-list tasks-but one appeared different. Anomalous sentence endings and words with semantic content in lists both showed coincident negative left frontotemporal and midline-anterior ERP foci, peaking at 332 msec for sentences and 316 msec for word lists. The most negative voltage obtained in the sentence task peaked at 386 msec and had a midline-posterior focus. A right frontotemporal focus developed after the midline-posterior focus and outlasted its duration. The most negative voltage for content words in lists was reached at 364 msec. The distribution of this ERP was extensive over the midline and appeared to differ from that observed in the sentence task. Modulation of language-related ERPs by word type and semantic priming was investigated using the word-list tasks, which required category-detection responses. Two novel findings were obtained: (1) The ERP distributions for words serving grammatical function and content words differed substantially in word lists. Even when devoid of any sentence context, function words presented significantly attenuated measures of N400 compared to content words. These findings support hypotheses that suggest a differential processing of content and function words. (2) Semantic priming functionally dissociated two ERP features in the 250-500 msec range. The later and most negative midline ERP feature (peaking at 364 msec) was attenuated by semantic priming. However, the earlier left frontotemporal feature (peaking at 316 msec) was enhanced by semantic priming. The isolation of this novel language-related ERF' that is sensitive to semantic manipulations has important consequences for temporal and mechanistic aspects of theories of language processing.
The timing of neural activity during shifts of spatial attention.
We developed a new experimental task to investigate the relative timing of neural activity during shifts of spatial attention with event-related potentials. The task enabled the investigation of nonlateralized as well as lateralized neural activity associated with spatial shifts. Participants detected target stimuli within one of two peripheral streams of visual letters. Colored letters embedded within the streams indicated which stream was to be used for target detection, signaling that participants should "hold" or "shift" their current focus of spatial attention. A behavioral experiment comparing performance in these focused-attention conditions with performance in a divided-attention condition confirmed the efficacy of the spatial cues. Another behavioral experiment showed that overt shifts of spatial attention were mainly complete by around 400 msec, placing an upper boundary for isolating neural activity that was instrumental in controlling spatial shifts. Event-related potentials recorded during a covert version of the focused-attention task showed a large amount of nonlateralized neural activity associated with spatial shifts, with significant effects starting around 330 msec. The effects started over posterior scalp regions, where they remained pronounced. Transient effects were also observed over frontal scalp regions. The results are compatible with a pivotal role of posterior parietal areas in initiating shifts of spatial attention.
Orienting attention to semantic categories.
We investigated the ability to orient attention to a complex, non-perceptual attribute of stimuli-semantic category. Behavioral consequences and neural correlates of semantic orienting were revealed and compared with those of spatial orienting, using event-related functional magnetic-resonance imaging. Semantic orienting significantly shortened response times to identify word stimuli, showing that it is possible to focus attention on non-perceptual attributes of stimuli to enhance behavioral performance. Semantic-orienting cues engaged parietal and frontal areas that were also involved in spatial orienting, but in addition engaged brain areas associated with semantic analysis of words, such as the left anterior inferior frontal cortex. These findings show that attentional orienting selectively engages brain areas with functional specialization for the predicted attributes. They also support the existence of a core frontoparietal network, which controls attentional orienting in speeded response tasks independently of the type of expectations, interacting with task-relevant functionally specialized areas to optimize perception and action.
Semantic priming of different affective categories.
The authors investigated affective semantic priming using a lexical decision task with 4 affective categories of related word pairs: neutral, happy, fearful, and sad. Results demonstrated a striking and reliable effect of affective category on semantic priming. Neutral and happy prime-targets yielded significant semantic priming. Fearful pairs showed no or modest priming facilitation, and sad primes slowed reactions to sad targets. A further experiment established that affective primes do not have generalized facilitatory-inhibitory effects. The results are interpreted as showing that the associative mechanisms that support semantic priming for neutral words are also shared by happy valence words but not for negative valence words. This may reflect increased vigilance necessary in adverse contexts or suggest that the associative mechanisms that bind negative valence words are distinct.