Mark W. Greenlee

Working memory in primate sensory systems

Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions — such as object motion in the visual system or the frequency of a sound in the auditory system — are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.

The Processing of First- and Second-Order Motion in Human Visual Cortex Assessed by Functional Magnetic Resonance Imaging (fMRI)

We have examined the activity levels produced in various areas of the human occipital cortex in response to various motion stimuli using functional magnetic resonance imaging (fMRI) methods. In addition to standard luminance-defined (first-order) motion, three types of second-order motion were used. The areas examined were the motion area V5 (MT) and the following areas that were delineated using retinotopic mapping procedures: V1, V2, V3, VP, V3A, and a new area that we refer to as V3B. Area V5 is strongly activated by second-order as well as by first-order motion. This activation is highly motion-specific. Areas V1 and V2 give good responses to all motion stimuli, but the activity seems to be related primarily to the local spatial and temporal structure in the image rather than to motion processing. Area V3 and its ventral counterpart VP also respond well to all our stimuli and show a slightly greater degree of motion specificity than do V1 and V2. Unlike V1 and V2, the response in V3 and VP is significantly greater for second-order motion than for first-order motion. This trend is evident, but less marked, in V3A and V3B and absent in V5. The results are consistent with the hypothesis that first-order motion sensitivity arises in V1, that second-order motion is first represented explicitly in V3 and VP, and that V5 (and perhaps also V3A and V3B) is involved in further processing of motion information, including the integration of motion signals of the two types.

Attentional suppression of activity in the human visual cortex.

We have used fMRI to examine the nature of the changes that occur in the human visual cortex when an observer attends to a particular location in the visual image. Previous studies have shown that the magnitude of the response to a visual stimulus is increased when the observer attends to the stimulus. We show that, in addition, attention to a particular location results in a widespread suppression of activity levels at all other locations. This suggests that a key mechanism of attentional modulation may be that spontaneous (baseline) levels of neural activity are adjusted in a position-dependent manner across the entire visual field.

Spatial imagery in deductive reasoning: a functional MRI study

Various cognitive theories aim to explain human deductive reasoning: (1) mental logic theories claim syntactic language-based proofs of derivation, (2) the mental model theory proposes cognitive processes of constructing and manipulating spatially organized mental models, and (3) imagery theories postulate that such abilities are based on visual mental images. To explore the neural substrates of human deductive reasoning, we examined BOLD (blood oxygen level dependent) contrasts of twelve healthy participants during relational and conditional reasoning with whole-brain functional magnetic resonance imaging (fMRI). The results indicate that, in the absence of any correlated visual input, reasoning activated an occipitoparietal-frontal network, including parts of the prefrontal cortex (Brodmanns area, BA, 6, 9) and the cingulate gyrus (BA 32), the superior and inferior parietal cortex (BA 7, 40), the precuneus (BA 7), and the visual association cortex (BA 19). In the discussion, we first focus on the activated occipito-parietal pathway that is well known to be involved in spatial perception and spatial working memory. Second, we briefly relate the activation in the prefrontal cortical areas and in the anterior cingulate gyrus to other imaging studies on higher cognitive functions. Finally, we draw some general conclusions and argue that reasoners envisage and inspect spatially organized mental models to solve deductive inference problems.

Spatiotemporal Frequency and Direction Sensitivities of Human Visual Areas Measured Using fMRI

Using functional magnetic resonance imaging (fMRI) we have studied the variation in response magnitude, in each visual area (V1-V5), as a function of spatial frequency (SF), temporal frequency (TF) and unidirectional motion versus counterphase flicker. Each visual area was identified in each subject using a combination of retinotopic mapping fMRI and cortical flattening techniques. A drifting (or counterphasing) sinusoidal grating was used as the stimulus in a study in which we parametrically varied SF between 0.4 and 7 cycles/degree and TF between 0 and 18 Hz. For each experiment we constructed fMRI amplitude tuning curves, averaged across subjects, for each visual area. The tuning curves that resulted are consistent with the known physiological properties of cells in the corresponding macaque visual areas, previous functional imaging studies, and in the case of V1, the psychophysically determined contrast sensitivity functions for spatial and temporal frequency. In the case of V3A, the SF tuning functions obtained were more similar to those found in single cell studies of macaque V3 rather than macaque V3A. All areas showed at least a moderate preference for directed versus counterphasing motion with V5 showing the largest preference. Visual areas V1, V2, V3, and V3A showed more direction sensitivity at low spatial frequencies, while VP, V4, and V5 had the highest drifting versus counterphasing ratios for higher spatial frequencies.

The functional role of contrast adaptation

Prolonged inspection of high contrast sinewave gratings increases the contrast required to detect gratings having a similar spatial frequency and orientation. The functional role of such adaptation has, however, in the past, eluded disclosure. We here show that 5 min adaptation to a 2 c/deg sinewave grating of 0.8 contrast changes the observers ability to discriminate the contrast level of a subsequently presented grating of the same spatial frequency and orientation. Similar to the threshold elevation effect, the observers required more incremental contrast for background contrast levels between 0.1 and 0.4 following adaptation. However, for contrast levels above 0.5, the observers required less delta contrast, following adaptation, to correctly discriminate which of two gratings was incremented in contrast. A simple model for adaptation is proposed to account for the findings which is based on a shift in the semi-saturation constant of the detectors contrast-response function. According to this model, adaptation acts to linearize the underlying mechanisms response in the region near the prevailing contrast level.

Cortical activation evoked by visual mental imagery as measured by fMRI.

One of the major controversies in cognitive neuroscience is whether the primary visual cortex and nearby areas are involved in visual mental imagery. In an fMRI study we examined the brain activity of 10 healthy subjects under different task conditions: in the perception condition subjects saw complex geometrical shapes and had to decide whether other highlighted stimuli fell inside or outside the figure. In the imagery condition subjects saw only the highlighted stimuli and were instructed to imagine the previously studied geometrical shapes to solve the same task. Although the behavioral data show a distance effect that would be expected based on topographically organized mental images, the functional imaging data do not show increased activity in the primary visual cortex in the imagery condition. In the occipital cortex a slightly increased activity was found only in the visual association cortex (BA 19), whereas the highest activation was observed in the parietal cortex (BA 7 and 40). The results of the study do not support the assumption that the primary visual cortex is involved in visual mental imagery, but rather that a network of spatial subsystems and higher visual areas appears to be involved.

Experimental pain thresholds and plasma beta-endorphin levels during exercise

Experimental pain thresholds (electrical intracutaneous finger and dental pulp stimulation) and plasma hormone levels (beta-endorphin, cortisol, and catecholamines) were measured in ten healthy sportive men before, during, and after progressively more strenuous physical exercise. In a double-blind study conducted on two different days, 20 mg of the opioid-antagonist naloxone or placebo was administered prior to exercise. A significant pain threshold elevation was found during exercise for finger (ANOVA, P less than 0.004) and dental pulp stimulation (P less than 0.01). Pain threshold elevation was most pronounced during maximal exertion, at which time the subjects reported the greatest subjective fatigue. Thresholds remained elevated 10-15 min after the end of exercise, and, 60 min after exercise, thresholds returned to baseline values. The subjective magnitude estimation of suprathreshold stimuli was significantly reduced (P less than 0.0001) 5-10 min after exercise. Plasma beta-endorphin, cortisol, and catecholamines increased significantly (P less than 0.0005, all values) during exercise. Plasma beta-endorphin levels did not correlate significantly with pain thresholds (r = -0.37, NS). Naloxone failed to affect pain thresholds, although beta-endorphin and cortisol increased significantly more (P less than 0.02) during exercise after naloxone. It is concluded that short-term, exhaustive physical exercise can evoke a transient elevation in pain thresholds. This exercise-induced elevation in pain threshold does not, however, appear to be directly related to plasma endorphin levels.

Human cortical areas underlying the perception of optic flow: brain imaging studies.

In summary, we have reviewed electrophysiological and brain imaging studies of motion and optic-flow processing. Single-unit studies indicate that MST (V5a) is a site of optic-flow extraction and that this information can be used to guide pursuit eye movements and to estimate heading. The EEG and MEG studies point to a localized electrical dipole in occipitotemporal cortex evoked by visual motion. We have also discussed the evidence from functional imaging studies for response specificity of the rCBF and BOLD effects in posterior cortex to visual motion and optic flow. Focal attention modulates the amplitude of the BOLD signal evoked by visual motion stimulation. Retinotopic mapping techniques have been used to locate region borders within the visual cortex. Our results indicate that striate (V1) and extrastriate areas (V2, V3/V3a) respond robustly to optic flow. However, with exception of a more pronounced response in V3/V3a to random walk, we found little evidence for response selectivity with respect to flow type and disparity in these early visual areas. In a similar fashion, the human V5/V5a complex responds well to optic flow, but these responses do not vary significantly with the type of flow field and do not seem to depend on disparity. In contrast, the kinetic occipital area (KO/V3b) responds well to optic-flow information, and it is the only area that produces more pronounced activation to the disparity in the flow fields. These initial results are promising because they suggest that the fMRI method can be sensitive to changes in stimulus parameters that define flow fields. More work will be required to explore the extent to which these responses reflect the neuronal processing of optic flow. Eye position tracking is now possible during fMRI experiments. We have demonstrated that the eye movements affect the BOLD responses in motion-sensitive areas (Kimming et al., 1999). Further experiments in our laboratory are aimed at understanding the effects of eye movements on the neuronal coding of complex optic-flow fields (Schira et al., 1999).

Retention and disruption of motion information in visual short-term memory

Velocity discrimination thresholds for drifting luminance gratings were measured as a function of the time interval between test and reference gratings, using a two-interval, forced-choice procedure. Discrimination thresholds, expressed as Weber fractions (delta V/V), were independent of interstimulus intervals (ISIs) ranging from 1-30 s, demonstrating perfect short-term retention of velocity information. When a third grating was briefly presented halfway through a 10-s ISI, memory masking was observed. Discrimination thresholds in memory masking were unaffected by maskers of the same velocity but increased by 100% when test and masker velocity differed by a factor of 2. The results are interpreted with reference to a model where the short-term memory for simple stimulus attributes is assumed to be organized in terms of arrays of memory stores linked in a lateral inhibitory network.