Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex

Gamma activity to stationary grating stimuli was studied non-invasively using MEG recordings in humans. Using a spatial filtering technique, we localized gamma activity to primary visual cortex. We tested the hypothesis that spatial frequency properties of visual stimuli may be related to the temporal frequency characteristics of the associated cortical responses. We devised a method to assess temporal frequency differences between stimulus-related responses that typically exhibit complex spectral shapes. We applied this methodology to either single-trial (induced) or time-averaged (evoked) responses in four frequency ranges (0-40, 20-60, 40-80 and 60-100 Hz) and two time windows (either the entire duration of stimulus presentation or the first second following stimulus onset). Our results suggest that stimuli of varying spatial frequency induce responses that exhibit significantly different temporal frequency characteristics. These effects were particularly accentuated for induced responses in the classical gamma frequency band (20-60 Hz) analyzed over the entire duration of stimulus presentation. Strikingly, examining the first second of the responses following stimulus onset resulted in significant loss in stimulus specificity, suggesting that late signal components contain functionally relevant information. These findings advocate a functional role of gamma activity in sensory representation. We suggest that stimulus specific frequency characteristics of MEG signals can be mapped to processes of neuronal synchronization within the framework of coupled dynamical systems.

Attentional changes in pre-stimulus oscillatory activity within early visual cortex are predictive of human visual performance

Physiological and neuroimaging studies provide evidence to suggest that attentional mechanisms operating within the fronto-parietal network may exert top–down control on early visual areas, priming them for forthcoming sensory events. The believed consequence of such priming is enhanced task performance. Using the technique of magnetoencephalography (MEG), we investigated this possibility by examining whether attention-driven changes in cortical activity are correlated with performance on a line-orientation judgment task. We observed that, approximately 200 ms after a covert attentional shift towards the impending visual stimulus, the level of phase-resetting (transient neural coherence) within the calcarine significantly increased for 2–10 Hz activity. This was followed by a suppression of alpha activity (near 10 Hz) which persisted until the onset of the stimulus. The levels of phase-resetting, alpha suppression and subsequent behavioral performance varied between subjects in a systematic fashion. The magnitudes of phase-resetting and alpha-band power were negatively correlated, with high levels of coherence associated with high levels of performance. We propose that top–down attentional control mechanisms exert their initial effects within the calcarine through a phase-resetting within the 2–10 Hz band, which in turn triggers a suppression of alpha activity, priming early visual areas for incoming information and enhancing behavioral performance.

Attentional modulation of oscillatory activity in human visual cortex

The effects of attentional modulation on activity within the human visual cortex were investigated using magnetoencephalography. Chromatic sinusoidal stimuli were used to evoke activity from the occipital cortex, with attention directed either toward or away from the stimulus using a bar-orientation judgment task. For five observers, global magnetic field power was plotted as a function of time from stimulus onset. The major peak of each function occurred at about 120 ms latency and was well modeled by a current dipole near the calcarine sulcus. Independent component analysis (ICA) on the non-averaged data for each observer also revealed one component of calcarine origin, the location of which matched that of the dipolar source determined from the averaged data. For two observers, ICA revealed a second component near the parieto-occipital sulcus. Although no effects of attention were evident using standard averaging procedures, time-varying spectral analyses of single trials revealed that the main effect of attention was to alter the level of oscillatory activity. Most notably, a sustained increase in alpha-band (7-12 Hz) activity of both calcarine and parieto-occipital origin was evident. In addition, calcarine activity in the range of 13-21 Hz was enhanced, while calcarine activity in the range of 5-6 Hz was reduced. Our results are consistent with the hypothesis that attentional modulation affects neural processing within the calcarine and parieto-occipital cortex by altering the amplitude of alpha-band activity and other natural brain rhythms. © 2003 Elsevier Inc. All rights reserved.

A brief review of magnetic fields from the human visual system

Both the eye and brain generate magnetic fields when stimulated with a variety of visual cues. These magnetic fields can be measured with a magnetometer; a device which uses superconducting technology. The application of this technique to measuring the magnetooculogram, magnetoretinogram and visually evoked fields from the brain is described. So far the main use of this technique has been in pure research. Its potential for diagnosing ocular and neurological diseases is discussed.

Development and application of magnetoencephalographic methods in the investigation of the human visual system

This thesis is an exploration of the organisation and functioning of the human visual system using the non-invasive functional imaging modality magnetoencephalography (MEG). Chapters one and two provide an introduction to the ‘human visual system and magnetoencephalographic methodologies. These chapters subsequently describe the methods by which MEG can be used to measure neuronal activity from the visual cortex. Chapter three describes the development and implementation of novel analytical tools; including beamforming based analyses, spectrographic movies and an optimisation of group imaging methods. Chapter four focuses on the use of established and contemporary analytical tools in the investigation of visual function. This is initiated with an investigation of visually evoked and induced responses; covering visual evoked potentials (VEPs) and event related synchronisation/desynchronisation (ERS/ERD). Chapter five describes the employment of novel methods in the investigation of cortical contrast response and demonstrates distinct contrast response functions in striate and extra-striate regions of visual cortex. Chapter six use synthetic aperture magnetometry (SAM) to investigate the phenomena of visual cortical gamma oscillations in response to various visual stimuli; concluding that pattern is central to its generation and that it increases in amplitude linearly as a function of stimulus contrast, consistent with results from invasive electrode studies in the macaque monkey. Chapter seven describes the use of driven visual stimuli and tuned SAM methods in a pilot study of retinotopic mapping using MEG; finding that activity in the primary visual cortex can be distinguished in four quadrants and two eccentricities of the visual field. Chapter eight is a novel implementation of the SAM beamforming method in the investigation of a subject with migraine visual aura; the method reveals desynchronisation of the alpha and gamma frequency bands in occipital and temporal regions contralateral to observed visual abnormalities. The final chapter is a summary of main conclusions and suggested further work.

Functional neuroimaging and behavioural studies on global form processing in the human visual system

Magnetoencephalography (MEG), functional magnetic resonance imaging (fMRI) and behavioural experiments were used to investigate the neural processes underlying global form perception in human vision. Behavioural studies using Glass patterns examined sensitivity for detecting radial, rotational and horizontal structure. Neuroimaging experiments using either Glass patterns or arrays of Gabor patches determined the spatio-temporal neural responseto global form. MEG data were analysed using synthetic aperture magnetometry (SAM) to spatially map event-related cortical oscillatory power changes: the temporal sequencing of activity within a discrete cortical area was determined using a Morlet wavelet transform. A case study was conducted to determine the effects of strbismic amblyopia on global form processing: all other observers were normally-sighted. The main findings from normally-sighted observers were: 1) sensitivity to horizontal structure was less than for radial or rotational structure; 2) the neural response to global structure was a reduction in cortical oscillatory power (10-30 Hz) within a network of extrastriate areas, including V4 and V3a; 3) the extend of reduced cortical power was least for horizontal patters; 4) V1 was not identified as a region of peak activity with either MEG or fMRI. The main findings with the strabismic amblyope were: 1) sensitivity for detection of radial, rotational, and horizontal structure was reduced when viewed with the amblyopic- relative to the fellow- eye; 2) cortical power changes within V4 to the presentation of rotational Glass patterns were less when viewed with the amblyopic- compared with the fellow- eye. The main conclusions are: 1) a network of extrastriate cortical areas are involved in the analysis of global form, with the most prominent change in neural activity being a reduction in oscillatory power within the 10-30 Hz band; 2) in strabismic amblyopia, the neuronal assembly associated with form perception in extrastriate cortex may be dysfunctional, the nature of this dysfunction may be a change in the normal temporal pattern of neuronal discharges; 3) MEG, fMRI and behavioural measures support the notion that different neural processes underlie the perception of horizontal as opposed to radial or rotational structure.

The development of calibration and adaptive filtering procedures for neuromagnetic studies of human visual function

This thesis first considers the calibration and signal processing requirements of a neuromagnetometer for the measurement of human visual function. Gradiometer calibration using straight wire grids is examined and optimal grid configurations determined, given realistic constructional tolerances. Simulations show that for gradiometer balance of 1:104 and wire spacing error of 0.25mm the achievable calibration accuracy of gain is 0.3%, of position is 0.3mm and of orientation is 0.6°. Practical results with a 19-channel 2nd-order gradiometer based system exceed this performance. The real-time application of adaptive reference noise cancellation filtering to running-average evoked response data is examined. In the steady state, the filter can be assumed to be driven by a non-stationary step input arising at epoch boundaries. Based on empirical measures of this driving step an optimal progression for the filter time constant is proposed which improves upon fixed time constant filter performance. The incorporation of the time-derivatives of the reference channels was found to improve the performance of the adaptive filtering algorithm by 15-20% for unaveraged data, falling to 5% with averaging. The thesis concludes with a neuromagnetic investigation of evoked cortical responses to chromatic and luminance grating stimuli. The global magnetic field power of evoked responses to the onset of sinusoidal gratings was shown to have distinct chromatic and luminance sensitive components. Analysis of the results, using a single equivalent current dipole model, shows that these components arise from activity within two distinct cortical locations. Co-registration of the resulting current source localisations with MRI shows a chromatically responsive area lying along the midline within the calcarine fissure, possibly extending onto the lingual and cuneal gyri. It is postulated that this area is the human homologue of the primate cortical area V4.

Neuro-electromagnetic imaging of the human visual cortex

Methods of solving the neuro-electromagnetic inverse problem are examined and developed, with specific reference to the human visual cortex. The anatomy, physiology and function of the human visual system are first reviewed. Mechanisms by which the visual cortex gives rise to external electric and magnetic fields are then discussed, and the forward problem is described mathematically for the case of an isotropic, piecewise homogeneous volume conductor, and then for an anisotropic, concentric, spherical volume conductor. Methods of solving the inverse problem are reviewed, before a new technique is presented. This technique combines prior anatomical information gained from stereotaxic studies, with a probabilistic distributed-source algorithm to yield accurate, realistic inverse solutions. The solution accuracy is enhanced by using both visual evoked electric and magnetic responses simultaneously. The numerical algorithm is then modified to perform equivalent current dipole fitting and minimum norm estimation, and these three techniques are implemented on a transputer array for fast computation. Due to the linear nature of the techniques, they can be executed on up to 22 transputers with close to linear speedup. The latter part of the thesis describes the application of the inverse methods to the analysis of visual evoked electric and magnetic responses. The CIIm peak of the pattern onset evoked magnetic response is deduced to be a product of current flowing away from the surface areas 17, 18 and 19, while the pattern reversal P100m response originates in the same areas, but from oppositely directed current. Cortical retinotopy is examined using sectorial stimuli, the CI and CIm ;peaks of the pattern onset electric and magnetic responses are found to originate from areas V1 and V2 simultaneously, and they therefore do not conform to a simple cruciform model of primary visual cortex.

Neuromagnetic investigations of functional organisation within human visual cortex

This thesis describes a series of experimental investigations into the functional organisation of human visual cortex using neuromagnetometry.This technique combines good spatial and temporal resolution enabling identification of the location and temporal response characteristics of cortical neurones within alert humans. To activate different neuronal populations and cortical areas a range of stimuli were used, the parameters of which were selected to match the known physiological properties of primate cortical neurones. In one series of experiments the evoked magnetic response was recorded to isoluminant red/green gratings. Co-registration of signal and magnetic resonance image data indicated a contribution to the response from visual areas V1, V2 and V4. To investigate the spatio-temporal characteristics of neurones within area V1 the evoked response was recorded for a range of stimulus spatial and temporal frequencies. The response to isoluminant red/green gratings was dominated by a major component which was found to have bandpass spatial frequency tuning with a peak at 1-2 cycles/degree, falling to the level of the noise at 6-8 cycles/degree. The temporal frequency tuning characteristics of the response showed bimodal sensitivity with peaks at 0-1Hz and 4Hz. In a further series of experiments the luminance evoked response was recorded to red/black, yellow/black and achromatic gratings and in all cases was found to be more complex than the isoluminant chromatic response, comprising up to three distinct components. The major response peak showed bandpass spatial frequency tuning characteristics, peaking at 6-8 cycles/degree, falling to the level of the noise at 12-16 cycles/degree. The results provide evidence to suggest that within area V1 the same neuronal population encodes both chromatic and luminance information and has spatial frequency tuning properties consistent with single-opponent cells. Furthermore, the results indicate that cells within area V1 encode chromatic motion information over a wide range of temporal frequencies with temporal response characteristics suggestive of the existence of a sub-population of cells sensitive to high temporal frequencies.

Pattern integration in the normal and abnormal human visual system

The processing conducted by the visual system requires the combination of signals that are detected at different locations in the visual field. The processes by which these signals are combined are explored here using psychophysical experiments and computer modelling. Most of the work presented in this thesis is concerned with the summation of contrast over space at detection threshold. Previous investigations of this sort have been confounded by the inhomogeneity in contrast sensitivity across the visual field. Experiments performed in this thesis find that the decline in log contrast sensitivity with eccentricity is bilinear, with an initial steep fall-off followed by a shallower decline. This decline is scale-invariant for spatial frequencies of 0.7 to 4 c/deg. A detailed map of the inhomogeneity is developed, and applied to area summation experiments both by incorporating it into models of the visual system and by using it to compensate stimuli in order to factor out the effects of the inhomogeneity. The results of these area summation experiments show that the summation of contrast over area is spatially extensive (occurring over 33 stimulus carrier cycles), and that summation behaviour is the same in the fovea, parafovea, and periphery. Summation occurs according to a fourth-root summation rule, consistent with a “noisy energy” model. This work is extended to investigate the visual deficit in amblyopia, finding that area summation is normal in amblyopic observers. Finally, the methods used to study the summation of threshold contrast over area are adapted to investigate the integration of coherent orientation signals in a texture. The results of this study are described by a two-stage model, with a mandatory local combination stage followed by flexible global pooling of these local outputs. In each study, the results suggest a more extensive combination of signals in vision than has been previously understood.

Interocular suppression and contrast gain control in human vision

The human visual system combines contrast information from the two eyes to produce a single cyclopean representation of the external world. This task requires both summation of congruent images and inhibition of incongruent images across the eyes. These processes were explored psychophysically using narrowband sinusoidal grating stimuli. Initial experiments focussed on binocular interactions within a single detecting mechanism, using contrast discrimination and contrast matching tasks. Consistent with previous findings, dichoptic presentation produced greater masking than monocular or binocular presentation. Four computational models were compared, two of which performed well on all data sets. Suppression between mechanisms was then investigated, using orthogonal and oblique stimuli. Two distinct suppressive pathways were identified, corresponding to monocular and dichoptic presentation. Both pathways impact prior to binocular summation of signals, and differ in their strengths, tuning, and response to adaptation, consistent with recent single-cell findings in cat. Strikingly, the magnitude of dichoptic masking was found to be spatiotemporally scale invariant, whereas monocular masking was dependent on stimulus speed. Interocular suppression was further explored using a novel manipulation, whereby stimuli were presented in dichoptic antiphase. Consistent with the predictions of a computational model, this produced weaker masking than in-phase presentation. This allowed the bandwidths of suppression to be measured without the complicating factor of additive combination of mask and test. Finally, contrast vision in strabismic amblyopia was investigated. Although amblyopes are generally believed to have impaired binocular vision, binocular summation was shown to be intact when stimuli were normalized for interocular sensitivity differences. An alternative account of amblyopia was developed, in which signals in the affected eye are subject to attenuation and additive noise prior to binocular combination.

Colour and luminance interactions in the visual perception of motion

We sought to determine the extent to which red–green, colour–opponent mechanisms in the human visual system play a role in the perception of drifting luminance–modulated targets. Contrast sensitivity for the directional discrimination of drifting luminance–modulated (yellow–black) test sinusoids was measured following adaptation to isoluminant red–green sinusoids drifting in either the same or opposite direction. When the test and adapt stimuli drifted in the same direction, large sensitivity losses were evident at all test temporal frequencies employed (1–16 Hz). The magnitude of the loss was independent of temporal frequency. When adapt and test stimuli drifted in opposing directions, large sensitivity losses were evident at lower temporal frequencies (1–4 Hz) and declined with increasing temporal frequency. Control studies showed that this temporal–frequency–dependent effect could not reflect the activity of achromatic units. Our results provide evidence that chromatic mechanisms contribute to the perception of luminance–modulated motion targets drifting at speeds of up to at least 32°s-1. We argue that such mechanisms most probably lie within a parvocellular–dominated cortical visual pathway, sensitive to both chromatic and luminance modulation, but only weakly selective for the direction of stimulus motion.

The missing link:Analogous human and primate cortical gamma oscillations

Recent animal studies highlighting the relationship between functional imaging signals and the underlying neuronal activity have revealed the potential capabilities of non-invasive methods. However, the valuable exchange of information between animal and human studies remains restricted by the limited evidence of direct physiological links between species. In this study we used magnetoencephalography (MEG) to investigate the occurrence of 30-70 Hz (gamma) oscillations in human visual cortex, induced by the presentation of visual stimuli of varying contrast. These oscillations, well described in the animal literature, were observed in retinotopically concordant locations of visual cortex and show striking similarity to those found in primate visual cortex using surgically implanted electrodes. The amplitude of the gamma oscillations increases linearly with stimulus contrast in strong correlation with the gamma oscillations found in the local field potential (LFP) of the macaque. We demonstrate that non-invasive magnetic field measurements of gamma oscillations in human visual cortex concur with invasive measures of activation in primate visual cortex, suggesting both a direct representation of underlying neuronal activity and a concurrence between human and primate cortical activity. © 2005 Elsevier Inc. All rights reserved.

Fixed or variable noise in contrast discrimination? The jury's still out

The ability to distinguish one visual stimulus from another slightly different one depends on the variability of their internal representations. In a recent paper on human visual-contrast discrimination, Kontsevich et al (2002 Vision Research 42 1771 - 1784) re-considered the long-standing question whether the internal noise that limits discrimination is fixed (contrast-invariant) or variable (contrast-dependent). They tested discrimination performance for 3 cycles deg-1 gratings over a wide range of incremental contrast levels at three masking contrasts, and showed that a simple model with an expansive response function and response-dependent noise could fit the data very well. Their conclusion - that noise in visual-discrimination tasks increases markedly with contrast - has profound implications for our understanding and modelling of vision. Here, however, we re-analyse their data, and report that a standard gain-control model with a compressive response function and fixed additive noise can also fit the data remarkably well. Thus these experimental data do not allow us to decide between the two models. The question remains open. [Supported by EPSRC grant GR/S74515/01]

Human sensitivity to phase perturbations in natural images:A statistical framework

Fourier-phase information is important in determining the appearance of natural scenes, but the structure of natural-image phase spectra is highly complex and difficult to relate directly to human perceptual processes. This problem is addressed by extending previous investigations of human visual sensitivity to the randomisation and quantisation of Fourier phase in natural images. The salience of the image changes induced by these physical processes is shown to depend critically on the nature of the original phase spectrum of each image, and the processes of randomisation and quantisation are shown to be perceptually equivalent provided that they shift image phase components by the same average amount. These results are explained by assuming that the visual system is sensitive to those phase-domain image changes which also alter certain global higher-order image statistics. This assumption may be used to place constraints on the likely nature of cortical processing: mechanisms which correlate the outputs of a bank of relative-phase-sensitive units are found to be consistent with the patterns of sensitivity reported here.