Recent Stimulus History Research Articles

Recent stimulus history impacts the speed of response for a new stimulus

Recent stimulus history impacts the speed of response for a new stimulus

Serial dependence requires visual awareness: Evidence from continuous flash suppression.

The visual system often undergoes a relatively stable perception even in a noisy visual environment. This crucial function was reflected in a visual perception phenomenon-serial dependence, in which recent stimulus history systematically biases current visual decisions. Although serial dependence effects have been revealed in numerous studies, few studies examined whether serial dependence would require visual awareness. By using the continuous flash suppression (CFS) technique to render grating stimuli invisible, we investigated whether serial dependence effects could emerge at the unconscious levels. In an orientation adjustment task, subjects viewed a randomly oriented grating and reported their orientation perception via an adjustment response. Subjects performed a series of three type trial pairs. The first two trial pairs, in which subjects were instructed to make a response or no response toward the first trial of the pairs, respectively, were used to measure serial dependence at the conscious levels; the third trial pair, in which the grating stimulus in the first trial of the pair was masked by a CFS stimulus, was used to measure the serial dependence at the unconscious levels. One-back serial dependence effects for the second trial of the pairs were evaluated. We found significant serial dependence effects at the conscious levels, whether absence (Experiment 1) or presence (Experiment 2) of CFS stimuli, but failed to find the effects at the unconscious levels, corroborating the view that serial dependence requires visual awareness.

Encoding surprise by retinal ganglion cells.

The efficient coding hypothesis posits that early sensory neurons transmit maximal information about sensory stimuli, given internal constraints. A central prediction of this theory is that neurons should preferentially encode stimuli that are most surprising. Previous studies suggest this may be the case in early visual areas, where many neurons respond strongly to rare or surprising stimuli. For example, previous research showed that when presented with a rhythmic sequence of full-field flashes, many retinal ganglion cells (RGCs) respond strongly at the instance the flash sequence stops, and when another flash would be expected. This phenomenon is called the 'omitted stimulus response'. However, it is not known whether the responses of these cells varies in a graded way depending on the level of stimulus surprise. To investigate this, we presented retinal neurons with extended sequences of stochastic flashes. With this stimulus, the surprise associated with a particular flash/silence, could be quantified analytically, and varied in a graded manner depending on the previous sequences of flashes and silences. Interestingly, we found that RGC responses could be well explained by a simple normative model, which described how they optimally combined their prior expectations and recent stimulus history, so as to encode surprise. Further, much of the diversity in RGC responses could be explained by the model, due to the different prior expectations that different neurons had about the stimulus statistics. These results suggest that even as early as the retina many cells encode surprise, relative to their own, internally generated expectations.

Resource-rational account of sequential effects in human prediction.

An abundant literature reports on 'sequential effects' observed when humans make predictions on the basis of stochastic sequences of stimuli. Such sequential effects represent departures from an optimal, Bayesian process. A prominent explanation posits that humans are adapted to changing environments, and erroneously assume non-stationarity of the environment, even if the latter is static. As a result, their predictions fluctuate over time. We propose a different explanation in which sub-optimal and fluctuating predictions result from cognitive constraints (or costs), under which humans however behave rationally. We devise a framework of costly inference, in which we develop two classes of models that differ by the nature of the constraints at play: in one case the precision of beliefs comes at a cost, resulting in an exponential forgetting of past observations, while in the other beliefs with high predictive power are favored. To compare model predictions to human behavior, we carry out a prediction task that uses binary random stimuli, with probabilities ranging from 0.05 to 0.95. Although in this task the environment is static and the Bayesian belief converges, subjects' predictions fluctuate and are biased toward the recent stimulus history. Both classes of models capture this 'attractive effect', but they depart in their characterization of higher-order effects. Only the precision-cost model reproduces a 'repulsive effect', observed in the data, in which predictions are biased away from stimuli presented in more distant trials. Our experimental results reveal systematic modulations in sequential effects, which our theoretical approach accounts for in terms of rationality under cognitive constraints.

Boundary updating as a source of history effect on decision uncertainty

When sorting a sequence of stimuli into binary classes, current choices are often negatively correlated with recent stimulus history. This phenomenon-dubbed the repulsive bias-can be explained by boundary updating, a process of shifting the class boundary to previous stimuli. This explanation implies that recent stimulus history can also influence "decision uncertainty," the probability of making incorrect decisions, because it depends on the location of the boundary. However, there have been no previous efforts to elucidate the impact of previous stimulus history on decision uncertainty. Here, from the boundary-updating process that accounts for the repulsive bias, we derived a prediction that decision uncertainty increases as current choices become more congruent with previous stimuli. We confirmed this prediction in behavioral, physiological, and neural correlates of decision uncertainty. Our work demonstrates that boundary updating offers a principled account of how previous stimulus history concurrently relates to choice bias and decision uncertainty.

Serial dependence in facial identity perception and visual working memory.

Serial dependence (SD) refers to the effect in which a person's current perceptual judgment is attracted toward recent stimulus history. Perceptual and memory processes, as well as response and decisional biases, are thought to contribute to SD effects. The current study examined the processing stages of SD facial identity effects in the context of task-related decision processes and how such effects may differ from visual working memory (VWM) interactions. In two experiments, participants were shown a series of two sequentially presented face images. In Experiment 1, the two faces were separated by an interstimulus interval (ISI) of 1, 3, 6, or 10 s, and participants were instructed to reproduce the second face after a varying response delay of 0, 1, 3, 6, or 10 s. Results showed that SD effects occurred most consistently at ISI of 1 s and response delays of 1 and 6 s consistent with early and late stages of processing. In Experiment 2, the ISI was held constant at 1 s, and to separate SD from VWM interactions participants were post-cued to reproduce either the first or the second face. When the second face was the target, SD effects again occurred at response delays of 1 and 6 s, but not when the first face was the target. Together, the results demonstrates that SD facial identity effects occur independently of task-related processes in a distinct temporal fashion and suggest that SD and VWM interactions may rely on separate underlying mechanisms.

Input-specific synaptic depression shapes temporal integration in mouse visual cortex

Efficient sensory processing requires the nervous system to adjust to ongoing features of the environment. In primary visual cortex (V1), neuronal activity strongly depends on recent stimulus history. Existing models can explain effects of prolonged stimulus presentation but remain insufficient for explaining effects observed after shorter durations commonly encountered under natural conditions. We investigated the mechanisms driving adaptation in response to brief (100ms) stimuli in L2/3 V1 neurons by performing invivo whole-cell recordings to measure membrane potential and synaptic inputs. We find that rapid adaptation is generated by stimulus-specific suppression of excitatory and inhibitory synaptic inputs. Targeted optogenetic experiments reveal that these synaptic effects are due to input-specific short-term depression of transmission between layers 4 and 2/3. Thus, brief stimulus presentation engages a distinct adaptation mechanism from that previously reported in response to prolonged stimuli, enabling flexible control of sensory encoding across a wide range of timescales.

Independent short- and long-term dependencies in perception.

Perception is biased by stimulus history. Both long-term effects such as the central-tendency bias (CTB) and short-term effects such as serial dependence (SD) have been described, but research into the two has remained largely separate. The sources of these effects, however, are highly correlated in stimulus statistics, which can result in a misinterpretation of experimental data. We compared CTB and SD in the perception of color and line length. Observers judged the relative hue or length of consecutive stimuli in a delayed-matching task. Two interstimulus intervals were used to investigate whether elapsed time or the number of stimulus occurrences was more important for SD. We estimated biases by fitting psychometric functions to the data split based on the history features, and we also fit generalized linear mixed models with either CTB, SD, or both included as regressors. We found biases to both recent stimulus history and the cumulative average of stimulus values for both color and line length judgments. The strength and pattern of each of the biases depended on whether all sources of bias were included in the analysis. Within the range of interstimulus intervals tested, the number of intervening stimuli was more important than elapsed time for SD. We conclude that both SD and CTB independently affect perceptual judgments, and that one effect is not an artifact caused by the other. Failing to consider both effects in data analysis can give an erroneous picture of the phenomenon under study.

Nonlinear dynamics in auditory cortical activity reveal the neural basis of perceptual warping in speech categorization.

Surrounding context influences speech listening, resulting in dynamic shifts to category percepts. To examine its neural basis, event-related potentials (ERPs) were recorded during vowel identification with continua presented in random, forward, and backward orders to induce perceptual warping. Behaviorally, sequential order shifted individual listeners’ categorical boundary, versus random delivery, revealing perceptual warping (biasing) of the heard phonetic category dependent on recent stimulus history. ERPs revealed later (∼300 ms) activity localized to superior temporal and middle/inferior frontal gyri that predicted listeners’ hysteresis/enhanced contrast magnitudes. Findings demonstrate that interactions between frontotemporal brain regions govern top-down, stimulus history effects on speech categorization.

Brief Stimuli Cast a Persistent Long-Term Trace in Visual Cortex.

Visual processing is strongly influenced by recent stimulus history, a phenomenon termed adaptation. Prominent theories cast adaptation as a consequence of optimized encoding of visual information by exploiting the temporal statistics of the world. However, this would require the visual system to track the history of individual briefly experienced events, within a stream of visual input, to build up statistical representations over longer timescales. Here, using an openly available dataset from the Allen Brain Observatory, we show that neurons in the early visual cortex of the mouse indeed maintain long-term traces of individual past stimuli that persist despite the presentation of several intervening stimuli, leading to long-term and stimulus-specific adaptation over dozens of seconds. Long-term adaptation was selectively expressed in cortical, but not in thalamic, neurons, which only showed short-term adaptation. Early visual cortex thus maintains concurrent stimulus-specific memory traces of past input, enabling the visual system to build up a statistical representation of the world to optimize the encoding of new information in a changing environment.SIGNIFICANCE STATEMENT In the natural world, previous sensory input is predictive of current input over multisecond timescales. The visual system could exploit these predictabilities by adapting current visual processing to the long-term history of visual input. However, it is unclear whether the visual system can track the history of individual briefly experienced images, within a stream of input, to build up statistical representations over such long timescales. Here, we show that neurons in early visual cortex of the mouse brain exhibit remarkably long-term adaptation to brief stimuli, persisting over dozens of seconds, and despite the presentation of several intervening stimuli. The visual cortex thus maintains long-term traces of individual briefly experienced past images, enabling the formation of statistical representations over extended timescales.

Computational principles of neural adaptation for binaural signal integration.

Adaptation to statistics of sensory inputs is an essential ability of neural systems and extends their effective operational range. Having a broad operational range facilitates to react to sensory inputs of different granularities, thus is a crucial factor for survival. The computation of auditory cues for spatial localization of sound sources, particularly the interaural level difference (ILD), has long been considered as a static process. Novel findings suggest that this process of ipsi- and contra-lateral signal integration is highly adaptive and depends strongly on recent stimulus statistics. Here, adaptation aids the encoding of auditory perceptual space of various granularities. To investigate the mechanism of auditory adaptation in binaural signal integration in detail, we developed a neural model architecture for simulating functions of lateral superior olive (LSO) and medial nucleus of the trapezoid body (MNTB) composed of single compartment conductance-based neurons. Neurons in the MNTB serve as an intermediate relay population. Their signal is integrated by the LSO population on a circuit level to represent excitatory and inhibitory interactions of input signals. The circuit incorporates an adaptation mechanism operating at the synaptic level based on local inhibitory feedback signals. The model’s predictive power is demonstrated in various simulations replicating physiological data. Incorporating the innovative adaptation mechanism facilitates a shift in neural responses towards the most effective stimulus range based on recent stimulus history. The model demonstrates that a single LSO neuron quickly adapts to these stimulus statistics and, thus, can encode an extended range of ILDs in the ipsilateral hemisphere. Most significantly, we provide a unique measurement of the adaptation efficacy of LSO neurons. Prerequisite of normal function is an accurate interaction of inhibitory and excitatory signals, a precise encoding of time and a well-tuned local feedback circuit. We suggest that the mechanisms of temporal competitive-cooperative interaction and the local feedback mechanism jointly sensitize the circuit to enable a response shift towards contra-lateral and ipsi-lateral stimuli, respectively.

Adaptation to stimulus orientation in mouse primary visual cortex.

Information processing in the visual system is shaped by recent stimulus history, such that prolonged viewing of an adapting stimulus can alter the perception of subsequently presented test stimuli. In the tilt-after-effect, the perceived orientation of a grating is often repelled away from the orientation of a previously viewed adapting grating. A possible neural correlate for the tilt-after-effect has been described in cat and macaque primary visual cortex (V1), where adaptation produces repulsive shifts in the orientation tuning curves of V1 neurons. We investigated adaptation to stimulus orientation in mouse V1 to determine whether known species differences in orientation processing, notably V1 functional architecture and proportion of tightly tuned cells, are important for these repulsive shifts. Unlike the consistent repulsion reported in other species, we found that repulsion was only about twice as common as attraction in our mouse data. Furthermore, adapted responses were attenuated across all orientations. A simple model that captured key physiological findings reported in cats and mice indicated that the greater proportion of broadly tuned neurons in mice may explain the observed species differences in adaptation.

Linear Summation of Repulsive and Attractive Serial Dependencies: Orientation and Motion Dependencies Sum in Motion Perception.

Recent work from several groups has shown that perception of various visual attributes in human observers at a given moment is biased toward what was recently seen. This positive serial dependency is a kind of temporal averaging that exploits short-term correlations in visual scenes to reduce noise and stabilize perception. To date, this stabilizing "continuity field" has been demonstrated on stable visual attributes such as orientation and face identity, yet it would be counterproductive to apply it to dynamic attributes in which change sensitivity is needed. Here, we tested this using motion direction discrimination and predict a negative perceptual dependency: a contrastive relationship that enhances sensitivity to change. Surprisingly, our data showed a cubic-like pattern of dependencies with positive and negative components. By interleaving various stimulus combinations, we separated the components and isolated a positive perceptual dependency for motion and a negative dependency for orientation. A weighted linear sum of the separate dependencies described the original cubic pattern well. The positive dependency for motion shows an integrative perceptual effect and was unexpected, although it is consistent with work on motion priming. These findings suggest that a perception-stabilizing continuity field occurs pervasively, occurring even when it obscures sensitivity to dynamic stimuli.SIGNIFICANCE STATEMENT Recent studies show that visual perception at a given moment is not entirely veridical, but rather biased toward recently seen stimuli: a positive serial dependency. This temporal smoothing process helps perceptual continuity by preserving stable aspects of the visual scene over time, yet, for dynamic stimuli, temporal smoothing would blur dynamics and reduce sensitivity to change. We tested whether this process is selective for stable attributes by examining dependencies in motion perception. We found a clear positive dependency for motion, suggesting that positive perceptual dependencies are pervasive. We also found a concurrent negative (contrastive) dependency for orientation. Both dependencies combined linearly to determine perception, showing that the brain can calculate contrastive and integrative dependencies simultaneously from recent stimulus history when making perceptual decisions.

The I/O transform of a chemical sensor

A number of sensing technologies, using a variety of transduction principles, have been proposed for non-invasive chemical sensing. A fundamental problem common to all these sensing technologies is determining what features of the transducer's signal constitute a chemical fingerprint that allows for precise analyte recognition. Of particular importance is the need to extract features that are robust with respect to the sensor's age or stimulus intensity. Here, using pulsed stimulus delivery, we show that a sensor's operation can be modeled as a linear input-output (I/O) transform. The I/O transform is unique for each analyte and can be used to precisely predict a temperature-programmed chemiresistor's response to the analyte given the recent stimulus history (i.e. state of an analyte delivery valve being open or closed). We show that the analyte specific I/O transforms are to a certain degree stimulus intensity invariant and can remain consistent even when the sensor has undergone considerable aging. Significantly, the I/O transforms for a given analyte are highly conserved across sensors of equal manufacture, thereby allowing training data obtained from one sensor to be used for recognition of the same set of chemical species with another sensor. Hence, this proposed approach facilitates decoupling of the signal processing algorithms from the chemical transducer, a key advance necessary for achieving long-term, non-invasive chemical sensing.

Perceptual adaptation: Getting ready for the future

Perceptual systems continually adapt to changes in their sensory environment. Adaptation has been mainly thought of as a mechanism to exploit the spatiotemporal regularities of the sensory input in order to efficiently represent sensory information. Thus, most computational explanations for adaptation can be conceptualized as a form of Efficient coding. We propose a novel and more holistic explanation. We argue that perceptual adaptation is a process with which the perceptual system adjusts its operational regime to be best possible prepared for the future, i.e. the next sensory input. Crucially, we assume that these adjustments affect both the way the system represents sensory information (encoding) and how it interprets that information (decoding). We apply this idea in the context of a Bayesian observer model. More specifically, we propose that the perceptual system tries to predict the probability distribution from which the next sensory input is drawn. It does so by exploiting the fact that the recent stimulus history is generally a good predictor of the future and that the overall long-term stimulus distribution is stationary. We assume that this predicted probability distribution reflects the updated prior belief of the Bayesian observer. In addition, we assume that the system is adjusting its sensory representation according to the predicted future stimulus distribution via Efficient coding. Because this sensory representation directly constrains the likelihood function, we can define an optimal Bayesian observer model for any predicted distribution over the next sensory input. We demonstrate that this model framework provides a natural account of the reported adaptation after-effects for visual orientation and spatial frequency, both in terms of discrimination thresholds and biases. It also allows us to predict how these after-effects depend on the specific form of the short- and long-term input histories. Meeting abstract presented at VSS 2015

Spike timing precision changes with spike rate adaptation in the owl's auditory space map.

Spike rate adaptation (SRA) is a continuing change of responsiveness to ongoing stimuli, which is ubiquitous across species and levels of sensory systems. Under SRA, auditory responses to constant stimuli change over time, relaxing toward a long-term rate often over multiple timescales. With more variable stimuli, SRA causes the dependence of spike rate on sound pressure level to shift toward the mean level of recent stimulus history. A model based on subtractive adaptation (Benda J, Hennig RM. J Comput Neurosci 24: 113-136, 2008) shows that changes in spike rate and level dependence are mechanistically linked. Space-specific neurons in the barn owl's midbrain, when recorded under ketamine-diazepam anesthesia, showed these classical characteristics of SRA, while at the same time exhibiting changes in spike timing precision. Abrupt level increases of sinusoidally amplitude-modulated (SAM) noise initially led to spiking at higher rates with lower temporal precision. Spike rate and precision relaxed toward their long-term values with a time course similar to SRA, results that were also replicated by the subtractive model. Stimuli whose amplitude modulations (AMs) were not synchronous across carrier frequency evoked spikes in response to stimulus envelopes of a particular shape, characterized by the spectrotemporal receptive field (STRF). Again, abrupt stimulus level changes initially disrupted the temporal precision of spiking, which then relaxed along with SRA. We suggest that shifts in latency associated with stimulus level changes may differ between carrier frequency bands and underlie decreased spike precision. Thus SRA is manifest not simply as a change in spike rate but also as a change in the temporal precision of spiking.

A single mechanism of temporal integration unites neural adaptation and norm-based coding

What information is encoded in a cortical visual representation? That visual representations are distributed across the ventral temporal cortex is well established. fMRI adaptation studies demonstrate these neural codes are modulated by the perceptual similarity of sequential stimuli. Studies investigating prototype-based coding effects propose that neural responses are proportional to distinctiveness from a central reference, or prototype. In existing fMRI work, these two effects are considered independently. Here, we propose that these two effects arise as a consequence of a single mechanism of coding based upon temporal integration over recent stimulus history. Using a carry-over fMRI design, we show significant neural adaptation and prototype-based coding effects in a face-responsive region of interest in the right fusiform gyrus when effects are modeled discretely. By considering these effects as extremes of a single drifting norm model, we find that visual representations tend to encode identity in terms of intermediate stimulus history. Looking beyond the region of interest, we demonstrate that the effect of temporal context varies smoothly across the cortex, with the modulatory effect of recent visual history extending further back in time in a posterior to anterior fashion along the right ventral temporal cortex. These findings reframe two branches of the visual representation literature in terms of a unified encoding model. Importantly, this finding offers a perspective on the cortical topology of visual identity representations. We discuss these advances in terms of prior work related to the temporal qualities of visual stimuli. Meeting abstract presented at VSS 2014

Cascaded Effects of Spatial Adaptation in the Early Visual System

SummaryVirtually all stages of the visual system exhibit adaptation: neurons adjust their responses based on the recent stimulus history. While some of these adjustments occur at specific stages, others may be inherited from earlier stages. How do adaptation effects cascade along the visual system? We measured spatially selective adaptation at two successive stages in the mouse visual system: visual thalamus (LGN) and primary visual cortex (V1). This form of adaptation affected both stages but in drastically different ways: in LGN it only changed response gain, while in V1 it also shifted spatial tuning away from the adaptor. These effects, however, are reconciled by a simple model whereby V1 neurons summate LGN inputs with a fixed, unadaptable weighting profile. These results indicate that adaptation effects cascade through the visual system, that this cascading can shape selectivity, and that the rules of integration from one stage to the next are not themselves adaptable.

Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions

Recent stimulus history, or adaptation, can alter neuronal response properties. Adaptation effects have been characterized in a number of visually responsive structures, from the retina to higher visual cortex. However, it remains unclear whether adaptation effects across stages of the visual system take a similar form in response to a particular sensory event. This is because studies typically probe a single structure or cortical area, using a stimulus ensemble chosen to provide potent drive to the cells of interest. Here we adopt an alternative approach and compare adaptation effects in primary visual cortex (V1) and area MT using identical stimulus ensembles. Previous work has suggested these areas adjust to recent stimulus drive in distinct ways. We show that this is not the case: adaptation effects in V1 and MT can involve weak or strong loss of responsivity and shifts in neuronal preference toward or away from the adapter, depending on stimulus size and adaptation duration. For a particular stimulus size and adaptation duration, however, effects are similar in nature and magnitude in V1 and MT. We also show that adaptation effects in MT of awake animals depend strongly on stimulus size. Our results suggest that the strategies for adjusting to recent stimulus history depend more strongly on adaptation duration and stimulus size than on the cortical area. Moreover, they indicate that different levels of the visual system adapt similarly to recent sensory experience.

Adaptation maintains population homeostasis in primary visual cortex

Sensory systems exhibit mechanisms of neural adaptation, which adjust neuronal activity based on recent stimulus history. In primary visual cortex (V1), in particular, adaptation controls the responsiveness of individual neurons and shifts their visual selectivity. What benefits does adaptation confer to a neuronal population? We measured adaptation in the responses of populations of cat V1 neurons to stimulus ensembles with markedly different statistics of stimulus orientation. We found that adaptation serves two homeostatic goals. First, it maintains equality in the time-averaged responses across the population. Second, it maintains independence in selectivity across the population. Adaptation scales and distorts population activity according to a simple multiplicative rule that depends on neuronal orientation preference and on stimulus orientation. We conclude that adaptation in V1 acts as a mechanism of homeostasis, enforcing a tendency towards equality and independence in neural activity across the population.