Elsevier

NeuroImage

Volume 29, Issue 1, 1 January 2006, Pages 74-89
NeuroImage

Mapping multiple visual areas in the human brain with a short fMRI sequence

https://doi.org/10.1016/j.neuroimage.2005.07.033Get rights and content

Abstract

It is a fundamental insight of neuroscience that the cerebral cortex is divided into spatially separated and functionally distinct areas. In this study, we tried to map a large number of visual areas in individual subjects passively viewing a simple stimulus sequence during functional magnetic resonance imaging (fMRI) at 1.5 T. The blocked stimulus sequence contrasted static object photographs with video takes of movement through natural indoor and outdoor scenes, alternated with a control fixation task. Two runs of the 5-min sequence sufficed to invoke 29 distinguishable activations, 16 (13 bilateral) of which were observed in all 10 participants. At the ventral side, object responsive activations were organized along the lateral occipital–temporal surface and near the collateral and occipital–temporal sulci. The latter activations, corresponding to the lateral occipital complex, showed a different activation profile from those near the collateral sulcus, most likely corresponding to the color constancy areas V4/V8–V4α. A potentially new fusiform object area was seen in 6 subjects, even more anterior than the parahippocampal place area. At the dorsal side, consistent activations were mainly related to motion stimuli and included the well-known areas V3a, VIPS, POIPS, hV5+, STS and the cingulate sulcus. There was consistent activation in the parietal–occipital sulcus, containing the areas V6a and V6. In addition, all subjects showed activation in the superior–anterior precuneus. Thus, the short stimulus sequence robustly invoked multiple visual areas and can be used to map the organization of the visual system in normal and brain-damaged individuals.

Introduction

In monkeys, over 30 visual areas have been identified and their connectivity and functional properties were studied (Felleman and Van Essen, 1991, Van Essen, 2004). They exhibit a characteristic anatomical and functional organization, in which the majority of the retinal visual information enters the brain in the occipital lobe, passes through a number of retinotopically organized areas and segregates into two distinguishable but interconnected visual information streams extending along the dorsal and the ventral side of the brain, respectively.

Although much less is known about the human visual system, functional imaging studies in the last decade revealed a roughly similar organization in the human brain. Four successive polar representations of visual field quadrants were shown to exist in the occipital cortex through phase-encoded retinal stimulation (DeYoe et al., 1996, Sereno et al., 1995). Subsequent studies demonstrated the involvement of several cortical areas along the ventral occipital–temporal brain in various aspects of visual form analysis and color constancy (e.g., Bartels and Zeki, 2000, Kanwisher et al., 1996, Malach et al., 1995). Concurrent studies mapped the occipital–parietal–frontal networks involved in complex visual functions such as saccade control (Heide et al., 2001, Petit et al., 1997), visual attention (Astafiev et al., 2003, Beauchamp et al., 2001, Corbetta et al., 1998), spatial visual processing (Haxby et al., 1991, Podzebenko et al., 2002, Trojano et al., 2002) and motion perception (Sunaert et al., 1999, Orban et al., 2003).

The ability to map the location and extent of known visual areas in single subjects has been a powerful tool in the study of the normal visual system as well as the organization of the visual system in patients with brain abnormalities. Retinotopic mapping, for instance, has become a standard tool in most fMRI studies of the visual system as an objective guide in the interpretation of activation results (see, for instance, Hadjikhani et al., 1998, Tootell and Hadjikhani, 2001). In addition, retinotopic mapping has been useful in assessing the functional consequences of neural disorders, by visualizing the functional cortical correlate of damage to the retina, the visual pathway or cerebral cortex (Barnes et al., 2001, Baseler et al., 1999, Morland et al., 2001, Sunness et al., 2004).

Despite the usefulness of cortical mapping and current day knowledge of higher cortical visual areas, there is at present no efficient method for mapping multiple higher visual areas. Recently, Bartels and Zeki (2004) presented an interesting approach to mapping visual areas, based on a multivariate statistical analysis of the characteristic activation time course of different cortical areas under natural viewing conditions. Although the approach is promising, it requires longer visual exposure times (25 min). In addition, it requires an elaborate screening procedure to distinguish independent components representing cortical or subcortical functional units from potential artefacts, such as those induced by scanner noise, subject movement, breathing or artery-pulsation. Moreover, the screening procedure relies substantially on intersubject correlations of activation time courses and their rankings, making it less applicable to individual subject data.

Here, we present a different approach to mapping ventral and dorsal cortical visual areas. The method uses a simple blocked stimulus design and requires only 10 min of scan-time. Activations are identified in single subjects based on their anatomical location and differences in their functional properties. Data from 10 brains will be presented. These will illustrate the robustness of the method and will provide the basis for describing the normal distribution pattern of ventral and dorsal activations with the proposed paradigm.

Section snippets

Subjects

Ten healthy volunteers aged 19 to 30 years (six male and four female) participated in the study. All participants were right handed (average laterality score 0.968 on Annett's Handedness Questionnaire (Annett, 1970)) and had normal or corrected to normal vision (binocular grating orientation acuity of ≥30 at 57 cm (Stiers et al., 2003)). None had a history of neurological or psychiatric disease. Approval from the local ethics committee and informed consent from all participants were obtained.

Procedure

Ventral visual areas

Passive viewing of photographs of common objects compared to the control fixation condition (contrast “objects > fixation”) yielded a large and usually continuous cluster of activated voxels along the ventral occipital–temporal side of the brain. Eight bilateral clusters could be distinguished within this large activation. They are tabulated in Table 1 and their anatomical location is illustrated in Fig. 1. Seven of the eight clusters were found bilaterally in all 10 participants.

The

Discussion

Ten minutes of passively viewing a simple stimulus sequence with two blocked conditions alternated with a control task were sufficient to map 29 cortical visual areas in normal subjects and to study their anatomical and relative positions. Sixteen activations were seen in all 10 participants. The stimulus conditions were chosen to preferentially activate the cortical areas of the ventral and the dorsal visual streams. No effort was made to minimize overlap in visual features between the

Conclusion

One of the fundamental insights of neuroscience is that the cortex is divided into spatially separate and functionally distinct areas. Understanding the brain amounts to knowing what areas are in existence and understanding their function and how they relate to each other. Over 30 visual cortical areas have been delineated in the Macaque monkey and many studies have been devoted to establishing the human homologues of monkey visual areas (Orban et al., 2003, Orban et al., 2004, Van Essen, 2004

Acknowledgments

P. Stiers was supported by the K.U. Leuven Onderzoeksfonds grants OT/01/43, PDM/01/156 and PDM/03/251. L. Lagae is holder of the “UCB chair in cognitive dysfunctions in childhood” at the K.U. Leuven. The authors which to thank Erik Luyten of the AVNet-Audiovisuele Dienst K.U. Leuven for technical support in creating the visual stimuli.

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