Project 1: Investigation of the neural circuits subserving visual perception and attention

Supervised students

H. Bahmani (Neural Correlates of Binocular Rivalry in Parietal Cortex)

F.A.C. Azevedo (Effects of attention on neural processing in the striate cortex of non-human primates)

Q. Li (Neuronal Population Activity Underlying Multi-Stable Motion Perception)

Introduction and Scientific Aims

The spontaneous perceptual alternations experienced when viewing certain type of visual stimuli, e.g. the Necker cube or Rubin’s faces-and-vase illusion, offer an excellent opportunity to discern neural activity related to conscious perception from that underlying sensory information processing.  Initial electrophysiological studies of multistable perception were performed in feature and object selective areas, i.e. in the temporal visual pathway, and demonstrated a widespread inter-areal network of neurons that modulate their activities according to their preferences and as well as according to which stimulus is perceived or suppressed [1-3]. Yet, fMRI studies indicated that areas with little or no pattern selectivity within the spatial-information processing dorsal pathway might also be involved in multistable perception, and particularly in the initiation of perceptual reversals [4]. Yet, not surprisingly, the mechanisms inducing perceptual alternations and temporary coherent percepts remain unclear. Unclear is also the role of attention and other neuromodulatory processes that may influence perceptual reorganization. Combined physiology and MR imaging is a promising approach for tackling such questions at the neural population, that is, they permit assessment of effective inter-area connectivity and study of local physiological responses. Our goal in this project is to study the mechanisms that select, extract, and bind together the visual features presented in multistable displays into coherent visual percepts, and the way such mechanisms are affected by attention.

Methods

We perform multi-electrode (tetrodes, laminar probes) [5] recordings in awake, behaving non-human primates (Macaca mulatta) trained to report their subjective perception during the presentation of multistable stimuli like binocular rivalry and motion plaids (Fig. 1 A). These stimuli yield clearly distinct perceptual states and allow parametric control over the relative probability of different percepts. In some animals, we also employ simultaneous recording of electrophysiological signals and fMRI while they perform spatial attention tasks in high field scanners (Fig. 1 B) [6]. Our analysis approaches include neural population decoding, measurements of synchrony and coherence between single unit activity (SUA) and local field potentials (LFP), probabilistic inference and theoretical modeling.

Results and Preliminary Conclusions

Electrophysiological recordings in the lateral intraparietal area (LIP) indicate a potential role of this area in perceptual transitions during binocular rivalry. The recorded units typically showed an initial burst of activity around perceptual transitions both during congruent and incongruent stimulation (Fig. 1 C). Importantly, these sharp transients are eliminated in conditions where physical changes that do not induce a concomitant change in perception are introduced in the stimuli. The transient response of the recorded neurons typically has a short latency and is then followed by a separate sustained response that exhibits independent dynamics. While the initial transient response is almost always excitatory the sustained responses are excitatory in some cells and suppressive in others. Interestingly, the sustained responses during incongruent stimulation were clearly suppressed in comparison to congruent conditions (Fig. 1 D).  We speculate that the transient and sustained responses may reflect two separate underlying processes. The short latency response may reflect a fast sensory integration signal in a bottom-up manner, while the sustained activity may represent top-down influences originating from higher areas in the prefrontal cortex.

It follows that areas at the high end of the dorsal pathway may be involved in multistable perception in a different way in comparison with feature and object selective areas of the ventral visual stream. While a hierarchically increasing percentage of feature selective neurons in the ventral pathway modulate their activities in parallel with perception of their preferred and non-preferred patterns, parietal areas might perform substantially different functions like integrating information from different spatial locations and signaling its binding into a coherent percept. Our preliminary results from electrophysiological recordings in LIP suggest that a transient signal is present only when there is a concomitant change in perception. This transient signal might provide a trigger for constellations of feature selective units in the ventral pathway to reorganize their patterns of activation leading to a perceptual switch. In addition, the suppression of the sustained responses during incongruent stimulation may indicate inhibitory processes underlying the competition between different stimulus representations at higher order areas.

References

1.         Ungerleider LG, Galkin TW, Mishkin M (1983) Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey, J Comp Neurol 217(2) 137-57.

2.         Leopold, D.A., and Logothetis, N.K. (1999) Multistable phenomena: changing views in perception, Trends Cogn Sci 3, 254-264.

3.         Keliris GA, Logothetis NK, and Tolias AS (2010) The role of the primary visual cortex in perceptual suppression of salient visual stimuli. J Neurosci 30, 12353-12365.

4.         Lumer ED, Friston KJ, and Rees G (1998) Neural correlates of perceptual rivalry in the human brain Science 280, 1930-1934.

5.         Tolias AS, Ecker AS, Siapas AG, Hoenselaar A, Keliris GA and Logothetis NK (2007) Recording Chronically from the same Neurons in Awake, Behaving Primates Journal of Neurophysiology 98(6) 3780-3790.

6.         Keliris GA, Shmuel A, Ku S, Pfeuffer J, Oeltermann A, Steudel T, and Logothetis NK (2007) Robust controlled functional MRI in alert monkeys at high magnetic field: effects of jaw and body movements Neuroimage 36 (3) 550-570.

Figure 1 We train non-human primates to report their subjective perception during presentation of bistable stimuli through a mirror steroscope (A). In some experiments we perform simultaneous recordings of electrophysiological and fMRI signals in high field scanners while modulating the attentional state of the subjects (B). Comparison between two experimental conditions (C) demonstrates strong suppression during incongurent in comparison to congruent stimulation (D).

Project 2: Studies of cortical reorganization after injury in human and non-human primates

(funded by the 7^th Framework Program of the European Commission – Plasticise project)

Supervised students

Y. Shao (Visual cortical plasticity after V1 lesion and retina degeneration in macaque monkeys)

A. Papanikolaou (Population receptive field mapping in human subjects with visual cortical lesions)

Collaborators

Dr. S. Lee (Estimation of population receptive fields in the human visual cortex)

Prof. Dr. S.M. Smirnakis (Baylor Collage Medicine, Houston, TX)

Prof. Dr. med. Ulrich Schiefer (Institute for Ophthalmic Research, UKT, Tuebingen)

Introduction and Scientific Aims

Damage to the visual cortex as a result of stroke or other brain diseases can lead to a loss of conscious vision in part(s) of the visual field introducing a tremendous burden to the individual. While the ability of the cortex to reorganize after injury has been convincingly demonstrated in the somatosensory, motor and language domains, evidence for reorganization in the visual cortex remains controversial with some studies suggesting extensive reorganization [1] while others find little if any changes [2, 3]. Further understanding of the reorganization capabilities of the visual system is central in the search for options of rehabilitation and recovery. We aim to study cortical reorganization after central nervous system injury in the visual system of human and non-human primates to understand: a) how is retinotopic organization of early visual cortical areas changing after visual cortex injury, b) if and how the receptive fields of neurons in the healthy cortex are changing, and c) how is sensitivity to motion in visual areas (deprived from their major input) changing. Initially we evaluate the degree to which the above changes happen spontaneously. Our long-term goal is to develop and assess specific training strategies that can invoke and/or enhance useful reorganization in the visual system and ultimately increase the patients’ quality of life.

Methods

Currently, we perform fMRI experiments both in human and non-human primates (rhesus macaques) to map visual response properties in a number of visual areas. Our visual stimulation paradigms include retinotopic mapping using moving bar stimuli that can be also used to estimate the aggregate receptive field sizes of fMRI voxels with the pRF method [4]. In addition, we use full field flickering white noise stimuli that stimulate differentially the spatio-temporal components of the receptive fields providing additional information for the responses of these populations of cells. At a second stage we will introduce cortical lesions in primary visual cortex of rhesus macaques and study visual reorganization at the electrophysiological level.

Results and Preliminary Conclusions

We find that the retinotopic maps of the spared early visual areas in patients with cortical lesions remain stable in comparison to control subjects (Fig. 1 A-B). In some subjects we observed some changes in the response properties of higher visual areas like V3A and hV5/MT+. In monkeys, we were able to reproduce accurate retinotopic maps and receptive field sizes agreeing with previous electrophysiological investigations (Fig. 1 C-D). Our preliminary results indicate that no significant reorganization happens spontaneously in early visual areas after injury

References

1.       Baker CI, Peli E, Knouf N, Kanwisher NG (2005) Reorganization of visual processing in macular degeneration J Neurosci 25(3):614-8.

2.       Sunness JS, Liu T, Yantis S. (2004) Retinotopic mapping of the visual cortex using functional magnetic resonance imaging in a patient with central scotomas from atrophic macular degeneration Ophthalmology 111(8):1595-8.

3.       Smirnakis SM, Brewer AA, Schmid MC, Tolias AS, Schuz A, Augath M, Inhoffen W, Wandell BA, Logothetis NK (2005) Lack of long-term cortical reorganization after macaque retinal lesions Nature 435(7040):300-7.

4.       Dumoulin SO, Wandell BA (2008) Population receptive field estimates in human visual cortex Neuroimage 39(2):647-60.

Figure 1 We use retinotopic mapping and particularly the pRF method [4] to map receptive field properties both in human (A-B) and non-human primates (C-D). Panels A, C present color coded maps of the populations receptive field sizes in early visual areas on flattened cortical surfaces. Panels B, D demonstrate that population receptive fields increase linearly with eccentricity in different visual areas.

CURRICULUM VITAE