Factor structure of the human gamma band oscillatory response to visual (contrast) stimulation.

OBJECTIVE: Visual contrast stimulation evokes in man an oscillatory mass response at approximately 20.0-35.0 Hz, consistent with stimulus-dependent synchronous oscillations in multiunit animal recordings from visual cortex, but shorter in duration and phase-locked to stimulus. A factor analysis was applied to characterize the signal structure under stimulus conditions inducing an oscillatory response and to identify possible subcomponents in normal volunteers. METHODS: Contrast stimuli were gratings with a sinusoidal luminance profile (9.0 degrees; 5.0 cycle/degree; 80% contrast; reversal 1.06 Hz). The amplitude spectrum of the signal was computed by Discrete Fourier Transform (DFT) and the oscillatory response was separated from the corresponding visually evoked potential (VEP) by DFT high-pass filter at 19.0 Hz. Nine consecutive waves were identified in all subjects (60 volunteers), with amplitudes/latencies consistent with normative studies. A factor analysis was computed 1- in the frequency domain, on the amplitude values of the signal components (2 Hz resolution), and 2- in the time domain, on the latencies/amplitudes of the averaged VEP and oscillatory responses. RESULTS: (1) Two non-overlapping factors accounted for the approximately 2-20.0 and approximately 20.0-40.0 Hz signal components, with separation of the approximately 20.0-35.0 Hz oscillatory response from low frequency VEPs. (2) Two factors on latencies and one factor on amplitudes (independent of each other and from those of VEPs) accounted for the average approximately 20.0-35.0 Hz oscillatory response. CONCLUSIONS: The factor structure further indicates an oscillatory structure and some independence from conventional VEPs of the human oscillatory response to contrast, with a separation between the oscillatory response early and late waves possibly reflecting functional differences.     

Gamma responses and ERPs in a visual classification task.

OBJECTIVE: We examined event-related potentials (ERPs) and gamma range EEG activity in a visual classification task to assess which variables affect these responses. METHODS: Ten subjects silently counted the occurrence of rare Kanizsa squares (targets) among Kanizsa triangles and non-Kanizsa figures (standards). By applying a time-frequency analysis to the data and selectively calculating topographical maps of certain frequencies. RESULTS: We were able to find 3 different types of gamma responses to Kanizsa figures: an early phase-locked gamma response at 40 Hz in the N100 time range, late phase-locked gamma activity (200-300 ms) at 40 Hz and a continuous phase-locked gamma response at 80 Hz due to the monitor refresh frequency. The two 40 Hz responses were significantly higher for Kanizsa figures than for non-Kanizsa figures and within the Kanizsa figures were higher for the target figure than for the non-target. CONCLUSION: The phase-locking of these two responses, previously found also as non-phase-locked activity, could be synchronized due to the monitor flicker frequency. Also, our findings suggest that the gamma responses are not solely associated with the binding of stimulus features, but reflect some processes related to target processing.     

Gamma band activity in an auditory oddball paradigm studied with the wavelet transform.

OBJECTIVES: To examine the characteristics of evoked and induced gamma band oscillatory responses occurring during P300 development in an auditory oddball paradigm. METHODS: A time-frequency analysis method was applied to an auditory oddball paradigm in 7 healthy subjects. This method combines a multiresolution wavelet algorithm for signal extraction and the Gabor transform to represent the temporal evolution of the selected frequency components. Phase-locked or evoked activity and also non-phase-locked activity were computed for both standard and target stimuli. RESULTS: The gamma band frequency components differed between target and non-target stimuli processing. The study showed an early and mainly phase-locked oscillatory response appearing around 26--28 ms after both standard and target stimuli onset. This response showed a spectral peak around 44 Hz for both stimuli. A late oscillatory activity peaking at 37 Hz with a latency around 360 ms was observed appearing only for target stimuli. The latency of this late oscillatory activity had a high correlation (P=0.002) to the latency of the P300 wave. CONCLUSIONS: EEG signal analysis with wavelet transform allows the identification of an early oscillatory cortical response in the gamma frequency range, as well as a late P300-related response.     

Wavelet transform of the EEG reveals differences in low and high gamma responses to elementary visual stimuli.

Multiunit electrophysiological studies indicate that oscillatory activity is common in the awake mammalian central nervous system. Synchronous 20-80 Hz oscillations, so called gamma rhythms, have been proposed as a possible fundamental physiological mechanism of binding neuronal activity underlying object recognition. The purpose of this study was to determine whether or not gamma band oscillatory activity in the human brain is modulated by attributes of elementary visual stimulation. The experiment was performed on 7 normal subjects. Sinusoidal gratings were presented over a range of spatial frequencies. Evoked potentials were recorded over 5 surface electrodes placed in a horizontal occipital chain across the back of the head. Discrete wavelet transform was performed on the first 200 msec following stimulus onset on the average data of 256 sweeps. Power was analyzed with ANOVA across conditions. In our previous studies we have separated a "low" (14-28 Hz) and "high" (28-55 Hz) gamma band. The current results indicate that both gamma bands to full-field stimulation have the highest power at the midline (inion) electrode to a spatial frequency of 5.5 cpd, which is the peak spatial frequency from foveal psychophysical data. However, the spatial frequency bandwidth is considerably narrower in the HG than in the LG band. Occipital spatial frequency tuning of the massed high gamma response is narrower than the tuning of individual cortical neurons. The bandwidth difference between low and high gamma band suggests that different frequency gamma range oscillations may represent not only different functional properties of visual processing, but may also reflect underlying differences in excitatory and postsynaptic inhibitory circuits shaping the contrast sensitivity of the human observer. Our study emphasizes the importance of elementary visual filter properties for gamma responses and the need to subdivide gamma frequency ranges according to functional properties.     

The influence of pattern size on amplitude, latency and wave form of retinal and cortical potentials elicited by checkerboard pattern reversal and stimulus onset-offset.

Transient pattern electroretinograms (PERGs) and visual evoked potentials (VEPs) were recorded with checkerboard pattern reversal and equiluminance stimulus onset-offset, elicited by a high quality moving mirror stimulator. Different sized checkerboard patterns (0.35-4.2 c/deg) were used as stimulus patterns. The wave forms of the equiluminance stimulus onset responses were similar to ERGs evoked with luminance decrease and the stimulus offset PERGs were like ERGs elicited by luminance increase. The PERG c wave and the VEP showed spatial frequency tuning with pattern reversal and stimulus offset. Spatial frequency tuning was not detectable with PERG a and b waves. Pattern reversal and stimulus onset evoked PERGs had no major spectral components above 40 Hz; stimulus offset evoked PERGs contained components up to 55.3 Hz. Retino-cortical time--measured as a latency difference of the PERG b wave to VEP P100--was identical with pattern reversal and stimulus onset and about 12 msec longer with stimulus offset. Our results suggest that the 3 stimulation modes, reversal, onset and offset induce different types of processing at the retinal and cortical levels. PERG a and b waves to our high luminance/contrast stimuli contain no pattern specific information and the c waves are the sum of luminance and pattern specific responses.     

Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study.

OBJECTIVE: To further evaluate the potential of slew-rate limiting amplifiers to record electrophysiological signals in spite of concurrent transcranial magnetic stimulation (TMS), and to explore the effects of single-pulse TMS on electroencephalographic (EEG) correlates of functional brain activity. METHODS: Visual-evoked potentials (VEPs) to checkerboards were recorded in 7 right-handed subjects, while single-pulse TMS was applied to the occipital pole either at visual stimulus onset, during the build-up or at the expected peak of the early VEP component P1 (VIS&TMS). Timing of TMS was individually adjusted based on each subject's VEP-latency. A condition of TMS without concurrent visual stimulation (TMS(alone)) served for subtraction purposes (VIS&TMS minus TMS(alone)) to partial out TMS-related contaminations of the EEG signal. RESULTS: When TMS was applied at visual stimulus onset, VEPs (as calculated by subtraction) perfectly matched control VEPs to visual stimulation alone. TMS at around P1, in contrast, modified the targeted (P1) and the subsequent VEP component (N1), independently of whether TMS was given at build-up or peak. CONCLUSIONS: The retrieval of regular VEPs with concomitant TMS at visual stimulus onset suggests that the employed EEG system and subtraction procedure are suited for combined EEG-TMS studies. The VEP changes following TMS at around P1 provide direct clues on the temporal dynamics of TMS pulse effects on functional activity in the human brain. Our data suggest effects of relatively long duration (approximately 100 ms) when TMS is applied while functional neuronal activity evolves.     

Threat modulates neural responses to looming visual stimuli

Objects on a collision course with an observer produce a specific pattern of optical expansion on the retina known as looming, which in theory exactly specifies the time‐to‐collision (TTC) of approaching objects. It was recently demonstrated that the affective content of looming stimuli influences perceived TTC, with threatening objects judged as approaching sooner than non‐threatening objects. Here, the neural mechanisms by which perceived threat modulates spatiotemporal perception were investigated. Participants judged the TTC of threatening (snakes, spiders) or non‐threatening (butterflies, rabbits) stimuli, which expanded in size at a rate indicating one of five TTCs. Visual‐evoked potentials (VEPs) and oscillatory neural responses measured with electroencephalography were analysed. The arrival time of threatening stimuli was underestimated compared with non‐threatening stimuli, though an interaction suggested that this underestimation was not constant across TTCs. Further, both speed of approach and threat modulated both VEPs and oscillatory responses. Speed of approach modulated the N1 parietal and oscillations in the beta band. Threat modulated several VEP components (P1, N1 frontal, N1 occipital, early posterior negativity and late positive potential) and oscillations in the alpha and high gamma band. The results for the high gamma band suggest an interaction between these two factors. Previous evidence suggests that looming stimuli activate sensorimotor areas, even in the absence of an intended action. The current results show that threat disrupts the synchronization over the sensorimotor areas that are likely activated by the presentation of a looming stimulus.     

Age effects on visual EEG responses reveal distinct frontal alpha networks.

OBJECTIVES: The present study aimed to describe the effect of aging on single-trial visual alpha responses. METHODS: Visual evoked potentials were recorded at F3, Cz, P3, and O1 in 12 young (20-30-year-olds) and in 10 middle-aged adults (50-55-year-olds). Slow (7-10 Hz) and fast (10-15 Hz) alpha frequency bands were analyzed. Three parameters of single alpha responses were assessed for the 0-300 ms period after stimulus: (i) maximal single-sweep amplitude; (ii) phase-locking with stimulus, and (iii) enhancement of post-stimulus relative to pre-stimulus alpha activity. RESULTS: Ongoing alpha activity at anterior sites was larger in middle-aged subjects. Age differences in response amplitude depended on the anterior shift of ongoing alpha activity. Over fronto-central areas, the phase-locking of fast alpha responses was significantly increased, whereas the phase-locking of slow alpha responses was decreased in middle-aged compared to young adults, independently of amplitude. In contrast to slow alpha responses, frontal and occipital fast alpha responses were interrelated. CONCLUSIONS: These observations are in accordance with previous findings from the auditory modality implying that the age-related changes in frontal alpha oscillations are modality-independent. Slow and fast frontal alpha responses were affected differentially by the age, which might reflect the activations of functionally distinct alpha networks.     

Functional properties of sub-bands of oscillatory brain waves to pattern visual stimulation in man.

The scalp recorded transient visual evoked potential (VEP) represents the massed activity of a large number of neurons of the human visual cortex. Animal studies show that intracerebrally-recorded high frequency electrical activity represents binding between neurons participating in a cooperative response. We evaluated the relationship between scalp recorded high frequency activity and transient VEPs elicited by a repetitive (grating) pattern. Stimuli were 1 and 4 cycles/degree sinusoidal gratings, presented in an on/off mode. Following conventional averaging, the discrete wavelet transform (DWT) was applied. Multi-resolution decomposition was used to divide the responses into 6 orthogonal frequency bands. The results show that high frequency oscillatory activity in the beta and gamma frequency range is closely related in time to the N70 peak of the simultaneous VEP. Power in both bands is modulated by spatial frequency. Beta range response to hemifield stimulation recorded over a chain of electrodes over the occipital area lateralizes in the same manner as N70, while gamma range activity is insensitive to lateralization and is more closely linked to foveal stimulation. This dissociation between beta and gamma range activity suggests that different bands of high frequency oscillatory activity in humans, linked to visual stimulation, may represent different aspects of visual processing.     

Abnormal early stages of task stimulus processing in children with attention-deficit hyperactivity disorder--evidence from event-related gamma oscillations.

OBJECTIVES: Attention-related differences in early stages of stimulus processing were assessed in healthy controls and children with attention-deficit hyperactivity disorder (ADHD) by analyzing phase-locked gamma band (31-63 Hz) responses to auditory stimuli in a selective-attention task. METHODS: A total of 28 children aged 9-12 years (ADHD and matched healthy controls) pressed a button in response to each target stimulus presented at the attended side (right or left). Auditory gamma band responses (GBRs) within 0-120 ms were analyzed at 8 electrodes with wavelet transform. Effects of attended channel, stimulus type, and group were evaluated for GBR power and phase-locking. RESULTS: For both groups, GBRs had a frontal-central distribution, were significantly larger and more strongly phase-locked to target than to non-target stimuli, and did not differentiate the attended from the unattended channel. ADHD children produced larger and more strongly phase-locked GBRs than controls only to right-side stimuli, irrespective of whether these were the attended or the ignored stimuli. CONCLUSIONS: The association between auditory GBR and motor task stimulus in children suggests that phase-locked gamma oscillations may reflect processes of sensory-motor integration. ADHD-related deviations of GBRs indicate that early mechanisms of auditory stimulus processing are altered in ADHD, presumably as a result of impaired motor inhibition.     

Equiluminant red-green and blue-yellow VEPs in multiple sclerosis.

The primate visual system is composed by two color-opponent pathways--red-green (R-G) and blue-yellow (B-Y)--subserved by the so-called parvo- and koniocellular streams respectively. The authors' aim was to compare the relative involvement of chromatic visual subsystems in multiple sclerosis (MS). In 30 MS patients with different forms of MS they recorded visual evoked potentials (VEPs) to onset (300 msec) and offset (700 msec) of equiluminant R-G and B-Y sinusoidal gratings of different contrast (90% and 25%). Equiluminance was established psychophysically by establishing the R-G and the B-Y color ratio at which chromatic gratings alternating at 15 and 10 Hz respectively had minimum visibility. The negative wave at stimulus onset with a peak latency of 120 to 160 msec was evaluated. Ordinary VEPs to luminance (LUM) contrast (black-white reversing checkerboards of 15' check size and 50% contrast) were also recorded for comparison. Latencies of R-G VEPs were abnormal in 53.3% and 58.3% of patients at 90% and 25% contrast respectively, whereas abnormal B-Y VEPs were 56.6% and 48.3%. Latencies of LUM VEPs were abnormal in 45% of patients. Interocular latency asymmetries were abnormal in 59.2% and 33.3% of patients for R-G, and 51.8% and 62.9% for B-Y. Latency asymmetries for LUM VEP were abnormal in 46.4% of patients. The higher rate of VEP abnormalities found with equiluminant chromatic stimuli compared with achromatic stimuli confirms the general vulnerability of color-opponent visual pathways in MS, even if the number of patients with abnormal findings was not significantly different when both test conditions were compared. VEPs to R-G and B-Y equiluminant stimuli appear to be involved approximately to the same extent.     

Repetition priming effects dissociate between miniature eye movements and induced gamma‐band responses in the human electroencephalogram

The role of induced gamma‐band responses (iGBRs) in the human electroencephalogram (EEG) is a controversial topic. On the one hand, iGBRs have been associated with neuronal activity reflecting the (re‐)activation of cortical object representations. On the other hand, it was shown that miniature saccades (MSs) lead to high‐frequency artifacts in the EEG that can mimic cortical iGBRs. We recorded EEG and eye movements simultaneously while participants were engaged in a combined repetition priming and object recognition experiment. MS rates were mainly modulated by object familiarity in a time window from 100 to 300 ms after stimulus onset. In contrast, artifact‐corrected iGBRs were sensitive to object repetition and object familiarity in a prolonged time window. EEG source analyses revealed that stimulus repetitions modulated iGBRs in temporal and occipital cortex regions while familiarity was associated with activity in parieto‐occipital regions. These results are in line with neuroimaging studies employing functional magnetic resonance imaging or magnetoencephalography. We conclude that MSs reflect early mechanisms of visual perception while iGBRs mirror the activation of cortical networks representing a perceived object.     

White noise effects on pattern-reversal visual evoked potentials.

Visual evoked potentials (VEPs) were recorded in 9 subjects from occipital and temporal leads. The stimulus was a checkerboard phase-reversed at the frequency of 1 Hz, binocularly viewed by the subject. VEPs were recorded during white noise stimulation (9 different levels of intensity) and without noise stimulation. P100 latency was not affected by the white noise stimulation, whereas the N75-P100 amplitude turned out to be affected by the simultaneous auditory stimulation with different patterns in relation to the site of the recording. The results are discussed in terms of general activation aroused by the white noise on visual information processing.     

High freuquency oscillatory activity in the human brain

Synchronized neural activity in animal visual cortex in the frequency range above 20 Hz, the gamma band, has been proposed as a signature of temporal feature binding. More and more research in humans by means of noninvasive electrophysiological recordings was stimulated by these studies. Here, research on evoked and induced gamma band activity in human EEG and MEG mainly in the auditory and visual modality is reviewed and their role in perceptual processes, feature integration and language processing is discussed. In addition, research on the attentional modulation of gamma band activity is reviewed. In contrast to evoked gamma band activity, which occurs right after stimulus onset, induced gamma band activity can be recorded with a latency of 200 to 400 ms and a frequency range of 30 to 95 Hz. Cumulative consistent experimental evidence allows us to conclude that gamma band activity in the human cortex is related to neuronal information processing and cognitive functions, e.g. memory processes. The findings are discussed in the light of different functional theories of induced gamma band activity.     

Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60-90 Hz) and beta (15-40 Hz) bands in the rat olfactory bulb

This study addressed the question of the possible functional relevance of two different oscillatory activities, beta and gamma (15-40 and 60-90 Hz, respectively) for perception and memory processes in olfactory areas of mammals. Local field potentials were recorded near relay olfactory bulb neurons while rats performed an olfactory discrimination task. Signals reflected the mass activity from this region and characteristics of oscillatory activities were used as an index of local synchrony. Beta and gamma oscillatory activities were quantified by time-frequency methods before during and after odour sampling. In rats early in their training, olfactory sampling was associated with a significant decrease in power in the gamma band in parallel with a weak but significant increase in the beta band (centred on 27 Hz). Several days later, in well-trained rats, the gamma oscillatory depression was significantly enhanced both in duration and amplitude. It appeared within the 500 ms time period preceding odour onset and was further reduced during the odour period. Concurrently the beta oscillatory response (now centred on 24 Hz) during odour sampling was amplified by a twofold factor. The beta band response was modulated according to the chemical nature of the stimuli and rat's behavioural response. This study showed for the first time that odour sampling in behaving animals is associated with a clear shift in the olfactory bulb neuronal activity from a gamma to a beta oscillatory regime. Moreover, the data stress the importance of studying the odour-induced beta activity and its relation to perception and memory.     

Stimulus‐dependent augmented gamma oscillatory activity between the functionally connected cortical neurons in the primary visual cortex

Neuronal assemblies typically synchronise within the gamma oscillatory band (30–80 Hz) and are fundamental to information processing. Despite numerous investigations, the exact mechanisms and origins of gamma oscillations are yet to be known. Here, through multiunit recordings in the primary visual cortex of cats, we show that the strength of gamma power (20–40 and 60–80 Hz) is significantly stronger between the functionally connected units than between the unconnected units within an assembly. Furthermore, there is increased frequency coherence in the gamma band between the connected units than between the unconnected units. Finally, the higher gamma rhythms (60–80 Hz) are mostly linked to the fast‐spiking neurons. These results led us to postulate that gamma oscillations are intrinsically generated between the connected units within cell assemblies (microcircuits) in relation to the stimulus within an emergent ‘50‐ms temporal window of opportunity’.     

Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task.

OBJECTIVE: The present study examined oscillatory brain activity of the EEG gamma band and event-related potentials (ERPs) with relation to the difficulty of a visual discrimination task. METHODS: Three tasks with identical stimulus material were performed by 9 healthy subjects. The tasks comprised a passive control task, and an easy and a hard visual discrimination task, requiring discrimination of the color of circles. EEG was recorded from 26 electrodes. A wavelet transform based on Morlet wavelets was employed for the analysis of gamma activity. RESULTS: Evoked EEG gamma activity was enhanced by both discrimination tasks as compared to the passive control task. Within the two discrimination tasks, the latency of the evoked gamma peak was delayed for the harder task. Higher amplitudes of the ERP components N170 and P300 were found in both discrimination tasks as compared to the passive task. The N2b, which showed a maximum activation at about 260 ms, was increased in the hard discrimination task as compared to the easy discrimination task. CONCLUSIONS: Our results indicate that early evoked gamma activity and N2b are related to the difficulty of visual discrimination processes. A delayed gamma activity in the hard task indicated a longer duration of stimulus processing, whereas the amplitude of the N2b directly indicates the level of task difficulty.     

Oscillatory correlates of retrieval-induced forgetting in recognition memory

Retrieval practice on a subset of previously studied material enhances later memory for practiced material but can inhibit memory for related unpracticed material. The present study examines the effects of prior retrieval practice on evoked (ERPs) and induced (oscillatory power) measures of electrophysiological activity underlying recognition of practiced and unpracticed words. Compared to control material, recognition of unpracticed words was characterized by reduced amplitudes of the P2 ERP component and by reduced early (200-400 msec) oscillatory theta power. The reduction in P2 amplitude was associated with decreased evoked theta power but not with decreased theta phase locking (phase-locking index). Recognition of unpracticed material was further accompanied by a reduction in occipital gamma power (>250 msec). In contrast, the beneficial effects of retrieval practice on practiced words were reflected by larger parietal ERP positivity (>500 msec) and by a stronger decrease in oscillatory alpha power in a relatively late time window (>700 msec). The results suggest that the beneficial and detrimental effects of retrieval practice are mediated by different processes. In particular, they suggest that reduced theta (4-7 Hz) and gamma (60-90 Hz) power reflect the specific effects of inhibitory processes on the unpracticed material's memory representation.     

Movement-related synchronization of gamma activity is lateralized in patients with dystonia

There is evidence for synchronization at frequencies both under 30 Hz and over 60-80 Hz in the so-called gamma frequency band in patients with Parkinson's disease (PD). Gamma activity increases after dopaminergic therapy and during voluntary movement, suggesting that it might be physiological and relate to motor processing in the basal ganglia (BG). We recorded local field potential (LFP) activity during a choice reaction time task in 11 patients with dystonia undergoing implantation of the internal globus pallidus for therapeutic stimulation. The spectral content of the LFP was averaged with respect to movement onset over 6-11 Hz, 18-25 Hz and 60-80 Hz, separately for responses ipsilateral and contralateral to movement. There was a perimovement increase in 60-80 Hz activity in the LFP, but only contralateral to movement. In contrast, low-frequency LFP activity decreased symmetrically during movement. This occurred earlier in the 18-25 Hz band than in the 6-11 Hz band, and was followed by a postmovement increase in oscillatory activity in the 18-25 Hz band that was contralateral to movement. The presence of a lateralized movement-related increase in gamma activity in the BG of patients with dystonia, similar to that recorded in patients with treated PD, suggests that this may be a residual feature of normal BG function. Moreover, the results provide further support for functional distinctions between BG oscillatory activities of different frequency.     

Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials.

OBJECTIVE: The present study aimed at examining the time course and topography of oscillatory brain activity and event-related potentials (ERPs) in response to laterally presented affective pictures. METHODS: Electroencephalography was recorded from 129 electrodes in 10 healthy university students during presentation of pictures from the international affective picture system. Frequency measures and ERPs were obtained for pleasant, neutral, and unpleasant pictures. RESULTS: In accordance with previous reports, a modulation of the late positive ERP wave at parietal recording sites was found as a function of emotional arousal. Early mid gamma band activity (GBA; 30-45 Hz) at 80 ms post-stimulus was enhanced in response to aversive stimuli only, whereas the higher GBA (46-65 Hz) at 500 ms showed an enhancement of arousing, compared to neutral pictures. ERP and late gamma effects showed a pronounced right-hemisphere preponderance, but differed in terms of topographical distribution. CONCLUSIONS: Late gamma activity may represent a correlate of widespread cortical networks processing different aspects of emotionally arousing visual objects. In contrast, differences between affective categories in early gamma activity might reflect fast detection of aversive stimulus features.