Recent Stimulus History Research Articles

Distinct Effects of Brief and Prolonged Adaptation on Orientation Tuning in Primary Visual Cortex

Recent stimulus history-adaptation-alters neuronal responses and perception. Previous electrophysiological and perceptual studies suggest that prolonged adaptation strengthens and makes more persistent the effects seen after briefer exposures. However, no systematic comparison has been made between the effects of adaptation lasting hundreds of milliseconds, which might arise during a single fixation, and the more prolonged adaptation typically used in imaging and perceptual studies. Here we determine how 0.4, 4, and 40 s of adaptation alters orientation tuning in primary visual cortex of anesthetized macaque monkeys, and how quickly responses recover after adapter offset. We measured responses to small (1.3°) and large (7.4°) gratings because previous work has shown that adaptation effects can depend on stimulus size. Adaptation with small gratings reduced responsivity and caused tuning to shift away from the adapter. These effects strengthened with more prolonged adaptation. For responses to large gratings, brief and prolonged adaptation produced indistinguishable effects on responsivity but caused opposite shifts in tuning preference. Recovery from adaptation was notably slower after prolonged adaptation, even when this did not induce stronger effects. We show that our results can be explained by an adaptation-induced weakening of surround suppression, the dynamics of this suppression, and differential effects of brief and prolonged adaptation across response epochs. Our findings show that effects do not simply scale with adaptation duration and suggest that distinct strategies exist for adjusting to moment-to-moment fluctuations in input and to more persistent visual stimuli.

Large-Scale Synchronized Activity during Vocal Deviance Detection in the Zebra Finch Auditory Forebrain

Auditory systems bias responses to sounds that are unexpected on the basis of recent stimulus history, a phenomenon that has been widely studied using sequences of unmodulated tones (mismatch negativity; stimulus-specific adaptation). Such a paradigm, however, does not directly reflect problems that neural systems normally solve for adaptive behavior. We recorded multiunit responses in the caudomedial auditory forebrain of anesthetized zebra finches (Taeniopygia guttata) at 32 sites simultaneously, to contact calls that recur probabilistically at a rate that is used in communication. Neurons in secondary, but not primary, auditory areas respond preferentially to calls when they are unexpected (deviant) compared with the same calls when they are expected (standard). This response bias is predominantly due to sites more often not responding to standard events than to deviant events. When two call stimuli alternate between standard and deviant roles, most sites exhibit a response bias to deviant events of both stimuli. This suggests that biases are not based on a use-dependent decrease in response strength but involve a more complex mechanism that is sensitive to auditory deviance per se. Furthermore, between many secondary sites, responses are tightly synchronized, a phenomenon that is driven by internal neuronal interactions rather than by the timing of stimulus acoustic features. We hypothesize that this deviance-sensitive, internally synchronized network of neurons is involved in the involuntary capturing of attention by unexpected and behaviorally potentially relevant events in natural auditory scenes.

Predictive context biases perceptual selection during binocular rivalry

Prediction may be a fundamental principle of sensory processing: it has been proposed that the brain continuously generates predictions about forthcoming sensory information. However, little is known about how prediction contributes to the selection of a conscious percept from among competing alternatives. Here, we used binocular rivalry to investigate the effects of prediction on perceptual selection. In binocular rivalry, incompatible images presented to the two eyes result in a perceptual alternation between the images, even though the visual stimuli remain constant. If predictive signals influence the competition between neural representations of rivalrous images, this influence should generate a bias in perceptual selection that depends on predictive context. To manipulate predictive context, we developed a novel binocular rivalry paradigm in which orthogonal rivalrous test gratings were immediately preceded by rotating gratings presented identically to the two eyes. One of the rivalrous gratings had an orientation that was consistent with the preceding rotation direction (it was the expected next image in the series), and the other had an inconsistent orientation. We found that human observers were more likely to perceive the consistent grating, suggesting that predictive context biased selection in favor of the predicted percept. This prediction effect depended on only recent stimulus history, and it could be dissociated from another stimulus history effect related to orientation-specific adaptation. Since binocular rivalry between orthogonal gratings is thought to be resolved at an early stage of visual processing, these results suggest that predictive signals may exist at low levels of the visual processing hierarchy and that these signals can bias conscious perception.

Predictive context biases perceptual selection during binocular rivalry

AbstractPrediction may be a fundamental principle of sensory processing, such that the brain continuously generates predictions about forthcoming sensory information. However, little is known about how prediction contributes to the selection of a conscious percept from among competing alternatives. Here, we used binocular rivalry to investigate the effects of prediction on perceptual selection. In binocular rivalry, incompatible images presented to the two eyes result in a perceptual alternation between the images, even though the visual stimuli remain constant. If predictive signals influence the competition between neural representations of rivalrous images, this influence should generate a bias in perceptual selection that depends on predictive context. To manipulate predictive context, we developed a novel binocular rivalry paradigm in which orthogonal rivalrous test gratings were immediately preceded by rotating gratings presented identically to the two eyes. One of the rivalrous gratings had an orientation that was consistent with the preceding rotation direction (it was the expected next image in the series), and the other had an inconsistent orientation. We found that human observers were more likely to perceive the consistent grating, suggesting that predictive context biased selection in favor of the predicted percept. This prediction effect depended on only recent stimulus history, and it could be dissociated from another stimulus history effect related to orientation-specific adaptation. Since binocular rivalry between orthogonal gratings is thought to be resolved at an early stage of visual processing, these results suggest that predictive signals may exist at low levels of the visual processing hierarchy and that these signals can bias conscious perception. In the future, this paradigm could be used to test whether visual percepts are generated from the combination of prior information and incoming sensory information according to Bayesian principles.

Conservative Decisions Guided by the Anterior Cingulate Cortex

Conservative Decisions Guided by the Anterior Cingulate Cortex

Neural processing of short-term recurrence in songbird vocal communication.

BackgroundMany situations involving animal communication are dominated by recurring, stereotyped signals. How do receivers optimally distinguish between frequently recurring signals and novel ones? Cortical auditory systems are known to be pre-attentively sensitive to short-term delivery statistics of artificial stimuli, but it is unknown if this phenomenon extends to the level of behaviorally relevant delivery patterns, such as those used during communication.Methodology/Principal FindingsWe recorded and analyzed complete auditory scenes of spontaneously communicating zebra finch (Taeniopygia guttata) pairs over a week-long period, and show that they can produce tens of thousands of short-range contact calls per day. Individual calls recur at time scales (median interval 1.5 s) matching those at which mammalian sensory systems are sensitive to recent stimulus history. Next, we presented to anesthetized birds sequences of frequently recurring calls interspersed with rare ones, and recorded, in parallel, action and local field potential responses in the medio-caudal auditory forebrain at 32 unique sites. Variation in call recurrence rate over natural ranges leads to widespread and significant modulation in strength of neural responses. Such modulation is highly call-specific in secondary auditory areas, but not in the main thalamo-recipient, primary auditory area.Conclusions/SignificanceOur results support the hypothesis that pre-attentive neural sensitivity to short-term stimulus recurrence is involved in the analysis of auditory scenes at the level of delivery patterns of meaningful sounds. This may enable birds to efficiently and automatically distinguish frequently recurring vocalizations from other events in their auditory scene.

When it's time for a change: Failures to track context in schizophrenia

IntroductionReduction of P300 event-related potential amplitude in schizophrenia is perhaps the most replicated biological reflection of the illness. P300 is typically elicited by infrequent deviant events that are imbedded in a series of identical frequent standard events. Deviants have features that explicitly distinguish them from standards, whereas standards can be distinguished from each other based on their local sequential probabilities within the stimulus series. The improbable occurrence of a standard should generate a P300, but only if the implicit local context generated by the recent stimulus history is processed. MethodTo assess the ability of schizophrenia patients to process this implicit contextual information, ERPs were elicited from 22 controls and 16 schizophrenia patients during an auditory oddball task containing infrequent target tones (15%) and novel distracter sounds (15%) imbedded pseudo-randomly in a series of standard tones (70%). Consecutively presented standards following deviant stimuli varied in sequential probability from p=1.0 for the 1st standard to p=0.16 for the 4th consecutive standard. ResultsPatients compared to controls demonstrated smaller P300 (P3a) to the fourth consecutive standard. However, in controls but not patients a contingent negative variation (CNV) was observed prior to the fourth standard, and an N2b/mismatch negativity (MMN) was observed following it. ConclusionsThese outcomes suggest that patients are deficient in using the implicit context established by recent stimulus history to anticipate that an otherwise standard stimulus was unlikely and its occurrence unexpected.

Predicting the Unpredictable: Weighted Averaging of Past Stimulus Timing Facilitates Ocular Pursuit of Randomly Timed Stimuli

In motor control, prediction of future events is vital for overcoming sensory-motor processing delays and facilitating rapid and accurate responses in a dynamic environment. In human ocular pursuit this is so pervasive that prediction of future target motion cannot easily be eliminated by randomizing stimulus parameters. We investigated the prediction of temporally randomized events during pursuit of alternating constant-velocity (ramp) stimuli in which the timing of direction changes varied unpredictably over a given range. Responses were not reactive; instead, smooth eye velocity began to decelerate in anticipation of each target reversal. In the first experiment, using a continuous-motion stimulus, we found that the time at which this occurred was relatively constant regardless of ramp duration, but increased as mean ramp duration of the range increased. Regression analysis revealed a quantitative association between deceleration timing and the previous two or three ramp durations in a trial, suggesting that recent stimulus history was used to create a running average of anticipatory timing. In the second experiment, we used discrete motion stimuli, with intervening periods of fixation, which allowed both target velocity and reversal timing to be varied, thereby decoupling ramp duration and displacement. This enabled us to confirm that the timing of anticipatory deceleration was based on the history of timing, rather than displacement, within the stimulus. We conclude that this strategy is used to minimize error amid temporal uncertainty, while simultaneously overcoming inherent delays in visuomotor processing.

Wide-dynamic-range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking.

An organism's ability to detect and discriminate sensory inputs depends on the recent stimulus history. For example, perceptual detection thresholds for a brief tone can be elevated by as much as 50 dB when following a masking stimulus. Previous work suggests that such forward masking is not a direct result of peripheral neural adaptation; the central pathway apparently modifies the representation in a way that further attenuates the input's response to short probe signals. Here, we show that much of this transformation is complete by the level of the inferior colliculus (IC). Single-neuron extracellular responses were recorded in the central nucleus of the awake marmoset IC. The threshold for a 20 ms probe tone presented at best frequency was determined for various masker-probe delays, over a range of masker sound pressure levels (SPLs) and frequencies. The most striking aspect of the data was the increased potency of forward maskers as their SPL was increased, despite the fact that the excitatory response to the masker was often saturating or nonmonotonic over the same range of levels. This led to probe thresholds at high masker levels that were almost always higher than those observed in the auditory nerve. Probe threshold shifts were not usually caused by a persistent excitatory response to the masker; instead we propose a wide-dynamic-range inhibitory mechanism locked to sound offset as an explanation for several key aspects of the data. These findings further delineate the role of subcortical auditory processing in the generation of a context-dependent representation of ongoing acoustic scenes.

Specialized neuronal adaptation for preserving input sensitivity.

Some neurons in auditory cortex respond to recent stimulus history by adapting their response functions to track stimulus statistics directly, as might be expected. In contrast, some neurons respond to loud sounds by adjusting their response functions away from high intensities and consequently remain sensitive to softer sounds. In marmoset monkey auditory cortex, the latter type of adaptation appears to exist only in neurons tuned to stimulus intensity.

What's That Sound? Auditory Area CLM Encodes Stimulus Surprise, Not Intensity or Intensity Changes

High-level sensory neurons encoding natural stimuli are not well described by linear models operating on the time-varying stimulus intensity. Here we show that firing rates of neurons in a secondary sensory forebrain area can be better modeled by linear functions of how surprising the stimulus is. We modeled auditory neurons in the caudal lateral mesopallium (CLM) of adult male zebra finches under urethane anesthesia with linear filters convolved not with stimulus intensity, but with stimulus surprise. Surprise was quantified as the logarithm of the probability of the stimulus given the local recent stimulus history and expectations based on conspecific song. Using our surprise method, the predictions of neural responses to conspecific song improved by 67% relative to those obtained using stimulus intensity. Similar prediction improvements cannot be replicated by assuming CLM performs derivative detection. The explanatory power of surprise increased from the midbrain through the primary forebrain and to CLM. When the stimulus presented was a random synthetic ripple noise, CLM neurons (but not neurons in lower auditory areas) were best described as if they were expecting conspecific song, finding the inconsistencies between birdsong and noise surprising. In summary, spikes in CLM neurons indicate stimulus surprise more than they indicate stimulus intensity features. The concept of stimulus surprise may be useful for modeling neural responses in other higher-order sensory areas whose functions have been poorly understood.

A perceptual architecture for sound lateralization in man

There are two general neurophysiological models of sound lateralization mechanisms which may be active in man. Both of the models are derived from studies in animals (one in barn owls, and one in mammals), and both have displayed some weakness in generalizability. One model advocates a population of neurons narrowly tuned to different interaural disparity values across the behaviorally relevant range, so that the cue value, and therefore the source azimuth, is represented by which neurons of the array are activated by the stimulus. The second model posits the existence of only two neural channels, each broadly tuned to interaural cue values favoring one acoustic hemifield, so that, especially for sources near the midline, cue value and therefore source azimuth is encoded by the relative activation of the two neural populations. The present article reviews three recent psychophysical studies, each using selective adaptation paradigms to probe sound lateralization mechanisms based on interaural disparities in normal human listeners. These experiments provided evidence on the frequency-specificity of interaural disparity coding and revealed its sensitivity to recent stimulus history. The data from those studies, however, also help distinguish the two lateralization models, and favor a perceptual architecture for sound lateralization in man based on the activity of two, hemifield-tuned azimuthal channels.

The effect of temporal context on the sustained pitch response in human auditory cortex.

Recent neuroimaging studies have shown that activity in lateral Heschl's gyrus covaries specifically with the strength of musical pitch. Pitch strength is important for the perceptual distinctiveness of an acoustic event, but in complex auditory scenes, the distinctiveness of an event also depends on its context. In this magnetoencephalography study, we evaluate how temporal context influences the sustained pitch response (SPR) in lateral Heschl's gyrus. In 2 sequences of continuously alternating, periodic target intervals and a more irregular baseline interval, the distinctiveness of the target was decreased in 1 of 2 ways--either by increasing the pitch strength of the baseline or by decreasing the pitch strength of the target. The results show that the amplitude of the SPR increases monotonically with the distinctiveness of the target. Moreover, SPR amplitude is greater for the sequence, where the pitch strength of the target is varied, compared with the condition, where the baseline is varied. Two subsequent experiments show that the amplitude of the SPR increases as duty cycle decreases, in a pitch "strength" contrast and in a pitch "value" contrast. These results indicate that the SPR adapts to recent stimulus history, enhancing the response to rare and brief events.

Recursive implementations of temporal filters for image motion computation.

Efficient algorithms for image motion computation are important for computer vision applications and the modelling of biological vision systems. Intensity-based image motion computation proceeds in two stages: the convolution of linear spatiotemporal filter kernels with the image sequence, followed by the non-linear combination of the filter outputs. If the spatiotemporal extent of the filter kernels is large, then the convolution stage can be very intensive computationally. One effective means of reducing the storage required and computation involved in implementing the temporal convolutions is the introduction of recursive filtering. Non-recursive methods require the number of frames of the image sequence stored at any given time to be equal to the temporal extent of the slowest temporal filter. In contrast, recursive methods encode recent stimulus history implicitly in the values of a small number of variables updated through a series of feedback equations. Recursive filtering reduces the number of values stored in memory during convolution and the number of mathematical operations involved in computing the filters' outputs. This paper extends previous recursive implementations of gradient- and correlation-based motion analysis algorithms [Fleet DJ, Langley K (1995) IEEE PAMI 17: 61-67; Clifford CWG, Ibbotson MR, Langley K (1997) Vis Neurosci 14: 741-749], describing a recursive implementation of causal band-pass temporal filters suitable for use in energy- and phase-based algorithms for image motion computation. It is shown that the filters' temporal frequency tuning curves fit psychophysical estimates of the temporal properties of human visual filters.

Mother perceptions and observed infant distress

Virtually 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.