Declan J. McKeefry

Induced Deficits in Speed Perception by Transcranial Magnetic Stimulation of Human Cortical Areas V5/MT+ and V3A

In this report, we evaluate the role of visual areas responsive to motion in the human brain in the perception of stimulus speed. We first identified and localized V1, V3A, and V5/MT+ in individual participants on the basis of blood oxygenation level-dependent responses obtained in retinotopic mapping experiments and responses to moving gratings. Repetitive transcranial magnetic stimulation (rTMS) was then used to disrupt the normal functioning of the previously localized visual areas in each participant. During the rTMS application, participants were required to perform delayed discrimination of the speed of drifting or spatial frequency of static gratings. The application of rTMS to areas V5/MT and V3A induced a subjective slowing of visual stimuli and (often) caused increases in speed discrimination thresholds. Deficits in spatial frequency discrimination were not observed for applications of rTMS to V3A or V5/MT+. The induced deficits in speed perception were also specific to the cortical site of TMS delivery. The application of TMS to regions of the cortex adjacent to V5/MT and V3A, as well as to area V1, produced no deficits in speed perception. These results suggest that, in addition to area V5/MT+, V3A plays an important role in a cortical network that underpins the perception of stimulus speed in the human brain.

Specialized and independent processing of orientation and shape in visual field maps LO1 and LO2

We identified human visual field maps, LO1 and LO2, in object-selective lateral occipital cortex. Using transcranial magnetic stimulation (TMS), we assessed the functions of these maps in the perception of orientation and shape. TMS of LO1 disrupted orientation, but not shape, discrimination, whereas TMS of LO2 disrupted shape, but not orientation, discrimination. This double dissociation suggests that specialized and independent processing of different visual attributes occurs in LO1 and LO2.

Functional evidence for cone-specific connectivity in the human retina

Physiological studies of colour vision have not yet resolved the controversial issue of how chromatic opponency is constructed at a neuronal level. Two competing theories, the cone‐selective hypothesis and the random‐wiring hypothesis, are currently equivocal to the architecture of the primate retina. In central vision, both schemes are capable of producing colour opponency due to the fact that receptive field centres receive input from a single bipolar cell – the so called ‘private line arrangement’. However, in peripheral vision this single‐cone input to the receptive field centre is lost, so that any random cone connectivity would result in a predictable reduction in the quality of colour vision. Behavioural studies thus far have indeed suggested a selective loss of chromatic sensitivity in peripheral vision. We investigated chromatic sensitivity as a function of eccentricity for the cardinal chromatic (L/M and S/(L + M)) and achromatic (L + M) pathways, adopting stimulus size as the critical variable. Results show that performance can be equated across the visual field simply by a change of scale (size). In other words, there exists no qualitative loss of chromatic sensitivity across the visual field. Critically, however, the quantitative nature of size dependency for each of the cardinal chromatic and achromatic mechanisms is very specific, reinforcing their independence in terms of anatomy and genetics. Our data provide clear evidence for a physiological model of primate colour vision that retains chromatic quality in peripheral vision, thus supporting the cone‐selective hypothesis.

Variant and invariant color perception in the near peripheral retina

Perceived shifts in hue that occur with increasing retinal eccentricity were measured by using an asymmetric color matching paradigm for a range of chromatic stimuli. Across nine observers a consistent pattern of hue shift was found; certain hues underwent large perceived shifts in appearance with increasing eccentricity, while for others little or no perceived shift was measured. In separate color naming experiments, red, blue, and yellow unique hues were found to be correlated with those hues that exhibited little or no perceptual shift with retinal eccentricity. Unique green, however, did not exhibit such a strong correlation. Hues that exhibited the largest perceptual shifts in the peripheral retina were found to correlate with intermediate hues that were equally likely to be identified by adjacent color naming mechanisms. However, once again the correlation was found to be weakest for the green mechanism. These data raise the possibility that perceptually unique hues are linked to color signals that represent the most reliable (minimally variant) chromatic information coming from the retina.

Sex-related differences in peripheral human color vision: a color matching study.

There has been much controversy as to whether there are sex-related differences in human color vision. While previous work has concentrated on testing the central visual field, this study compares male versus female color vision in the near peripheral retina. Male (n = 19) and female (n = 19) color normal observers who exhibited no significant differences either in the midpoints or the ranges of their Rayleigh matches were tested with a color matching paradigm. They adjusted hue and saturation of a 3° test spot (18° eccentricity) until it matched a 1° probe (1° eccentricity). Both groups demonstrated measurable shifts in the appearance of the peripheral color stimuli similar to those that have been previously reported. However, females showed substantially less saturation loss than males (p < 0.003) in the green-yellow region of color space. No significant differences were found in other regions of color space. This difference in the perceived saturation of color stimuli was minimally affected either by the inclusion or exclusion in the analysis of potential heterozygous female carriers of deutan color vision deficiencies. We speculate that this advantage of female over male color vision is conferred by M-cone polymorphism.

The segregation and integration of colour in motion processing revealed by motion after-effects

Analysis of the colour and motion of objects is widely believed to take place within segregated processing pathways in the primate visual system. However, it is apparent that this segregation cannot remain absolute and that there must be some capacity for integration across these sub-modalities. In this study, we have assessed the extent to which colour constitutes a separable entity in human motion processing by measuring the chromatic selectivity of two kinds of after-effect resulting from motion adaptation. First, the traditional motion after-effect, where prolonged inspection of a unidirectional moving stimulus results in illusory motion in the opposite direction, was found to exhibit a high degree of chromatic selectivity. The second type of after-effect, in which motion adaptation induces misperceptions in the spatial position of stationary objects, was completely insensitive to chromatic composition. This dissociation between the chromatic selectivities of these after-effects shows that chromatic inputs remain segregated at early stages of motion analysis, while at higher levels of cortical processing there is integration across chromatic, as well as achromatic inputs, to produce a unified perceptual output.

The Noninvasive Dissection of the Human Visual Cortex: Using fMRI and TMS to Study the Organization of the Visual Brain

The development of brain imaging techniques, such as fMRI, has given modern neuroscientists unparalleled access to the inner workings of the living human brain. Visual processing in particular has proven to be particularly amenable to study with fMRI. Studies using this technique have revealed the existence of multiple representations of visual space with differing functional roles across many cortical locations. Yet, although fMRI provides an excellent means by which we can localize and map different areas across the visual brain, it is less well suited to providing information as to whether activation within a particular cortical region is directly related to perception or behavior. These kinds of causal links can be made, however, when fMRI is combined with transcranial magnetic stimulation (TMS). TMS is a noninvasive technique that can bring about localized, transient disruption of cortical function and can induce functional impairments in the performance of specific tasks. When guided by the detailed localizing and mapping capabilities of fMRI, TMS can be used as a means by which the functional roles of different visual areas can be investigated. This review highlights recent insights that the techniques of fMRI and TMS have given us with regard to the function and contributions of the many different visual areas to human visual perception.

Simultaneous chromatic and luminance human electroretinogram responses

•  It has recently been shown that, with careful control over stimulation, the electroretinogram (ERG) can reflect the properties of the post‐receptoral parvocellular (P) and magnocellular (M) pathways, which are thought of as the respective substrates for red–green colour and luminance vision. •  Using a novel compound stimulus, which contains red–green colour information at the fundamental frequency and luminance information at the second harmonic, we were able to simultaneously record colour and luminance ERGs. •  In trichromats, the temporal tuning curves of these components reflected the known properties of the P and M systems, whereas the dichromats showed negligible chromatic response but a normal achromatic response. •  Parallel retinal processing that is relevant for vision can be reflected in the ERG.

L- and M-cone input to 12Hz and 30Hz flicker ERGs across the human retina

We recorded L‐ and M‐cone isolating ERGs from human subjects using a silent substitution technique at temporal rates of 12 and 30 Hz. These frequencies isolate the activity of cone‐opponent and non‐opponent post‐receptoral mechanisms, respectively. ERGs were obtained using a sequence of stimuli with different spatial configurations comprising; (1) circular stimuli of different sizes which increased in 10° steps up to 70°diameter, or (2) annular stimuli with a 70° outer diameter but with different sized central ablations from 10° up to 60°. L‐ and M‐cone isolating ERGs were obtained from five colour normal subjects using a DTL fibre electrode. Fourier analysis of the ERGs was performed and we measured the amplitude of the first harmonic of the response. For 12 Hz ERGs the L:M cone response amplitude ratio (L:MERG) was close to unity and remained stable irrespective of the spatial configuration of the stimulus. The maintenance of this balanced ratio points to the existence of cone selective input across the human retina for the L‐M cone opponent mechanism. For 30 Hz the L:MERG ratio was greater than unity but varied depending upon which region of the retina was being stimulated. This variation we consider to be a consequence of the global response properties of M‐cone ERGs rather than representing a real variation in L:M cone ratios across the retina.

The contribution of human cortical area V3A to the perception of chromatic motion: a transcranial magnetic stimulation study.

Area V3A was identified in five human subjects on both a functional and retinotopic basis using functional magnetic resonance imaging techniques. V3A, along with other visual areas responsive to motion, was then targeted for disruption by repetitive transcranial magnetic stimulation (rTMS) whilst the participants performed a delayed speed matching task. The stimuli used for this task included chromatic, isoluminant motion stimuli that activated either the L−M or S−(L+M) cone‐opponent mechanisms, in addition to moving stimuli that contained only luminance contrast (L+M). The speed matching task was performed for chromatic and luminance stimuli that moved at slow (2°/s) or faster (8°/s) speeds. The application of rTMS to area V3A produced a perceived slowing of all chromatic and luminance stimuli at both slow and fast speeds. Similar deficits were found when rTMS was applied to V5/MT+. No deficits in performance were found when areas V3B and V3d were targeted by rTMS. These results provide evidence of a causal link between neural activity in human area V3A and the perception of chromatic isoluminant motion. They establish area V3A, alongside V5/MT+, as a key area in a cortical network that underpins the analysis of not only luminance but also chromatically‐defined motion.