6. General discussion
6.4. Peripheral visual field representation in human parieto-occipital sulcus
We examined peripheral vision in studies II, IV, and VI. Stimulation system for wide visual field developed in study II enabled the mapping of medial occipital retinotopic areas up to 50 degrees of eccentricity. The results showed that areas V1-V3 extended to the anterior part of calcarine sulcus and the posterior bank of PO sulcus and suggested that human V6 with relatively large peripheral visual field representation is located in the posterior bank of PO sulcus. In addition, our results showed that the magnification factor describing the extent of the visual field representation is similar both in central and peripheral V1.
Results of studies IV and VI are in accordance with the association between peripheral vision and dorsal stream. In study IV saccades in darkness activated both frontal and parietal dorsal stream areas and peripheral visual field representations, suggesting a top-down signal from higher order dorsal stream areas to periphery of V1 and V2. On the other hand,
activation of dorsal stream areas in occipital and parietal lobe after peripheral stimulation in study VI, indicated feed-forward connections from peripheral retina to dorsal stream areas.
Previous knowledge from both human and monkey studies suggests that central and peripheral vision serve partially different functions in the visual system. Study IV demonstrates functional differences between central and peripheral vision by showing peripheral eye-movement –related responses in low-order retinotopic visual areas. In accordance with the study of Sylvester and Rees (2006), our results suggests that the peripheral activation may reflect movement processing, more specifically corollary discharge of a motor command (Sommer and Wurtz, 2008).
However, peripheral activation in study IV may also reflect more nonspecific top-down processes. In monkey V1, enhanced activity and synchrony of neurons before stimulus presentation facilitates stimulus detection (Supèr et al., 2003), whereas in humans, expecting a stimulus increases BOLD signal in V1 (Kastner et al., 1999) and task changes can cause BOLD signal increase in peripheral representations (Jack et al., 2006). Dorsal stream activation during eye-movements could send a resetting signal to low-order visual areas before the next trial. Thus the dorsal stream activation may prepare the visual cortex for a change in the information flow.
Previous studies (Baizer et al., 1991; Falchier et al., 2002; Gattass et al., 2005; Roberts et al., 2007) have suggested that the peripheral vision may be important for detecting sudden changes in the environment which may lead to a redirecting of activation flow. According to Bullier’s (2004b) proposal, the visual signal is first transmitted to the dorsal stream due to the short latencies of magnocellular neurons. This is followed by feedback signals which guide subsequent signal processing. Previous studies have provided evidence that the feedback circuits may extend from the periphery to the center. Central visual field representations contain information of the object presented in the peripheral visual field (Williams et al., 2008) and the perception of self-movement due to peripheral motion stimulus decreases visually evoked response in the central representations (Thilo et al., 2003). A feedback signal would require a fast activation after the initial peripheral
stimulation. Consistent with this, a peripheral stimulus activates the parieto-occipital cortex with a shorter latency than a central stimulus (Stephen et al., 2002) and stimulation of the peripheral visual field in study VI resulted in a stream of activation at a short latency in the dorso-medial stream areas in the human brain. Whether the peripheral vision and dorsal stream have a role in global to local guidance of visual information processing remains to be examined in the future studies.
7. Conclusions
This thesis investigated the processing of visual information in the human cortex. I measured neuromagnetic signals and BOLD responses during visual stimulation as well as during motor and cognitive tasks. Particularly, visual stimuli were designed to activate peripheral visual field representations and cognitive and motor tasks were designed to activate dorsal stream areas. The analysis of cortical responses concentrated on visual areas at low and intermediate levels of the anatomical hierarchy.
Modern imaging methods provide enormous opportunities to neuroscience by enabling studies of neural function in intact living human brain. This thesis examined some of the problems that may arise in imaging studies of human visual processing. First I examined the ambiguity of modelling neuromagnetic signal sources and showed, that even thought
nonsimultaneous sources can be located with good spatial and temporal accuracy a priori information is needed to differentiate spatially close and temporally overlapping sources. In addition, I attempted to overcome some of the physical limitations of stimulus design and developed an optical system that enables stimulation of peripheral visual field in a narrow magnet bore.
Peripheral vision is still relatively little studied and the second aim of my thesis was to study peripheral vision in human brain. I mapped the peripheral visual field representation of low-level retinotopic areas and showed functional differences between central and peripheral vision. In addition, my results suggest that peripheral representations in low-level areas are reciprocally connected with dorsal stream areas, especially within the dorso-medial stream.
In the monkey, the dorso-medial stream is involved in the processing of visuomotor actions.
My studies showed a rapid activation sequence and eye-movement related activation in the medial and dorsal occipital and parietal lobes. This stream of areas could represent the human dorso-medial stream suitable for a fast feed-forward-feedback analysis.
The third objective of my thesis was to study human V6. The results support previous findings that human V6 is located anterior to peripheral lower visual field representation of V2/V3 and is biased towards the peripheral visual field. My work shows that human V6 is motion sensitive and that it is related to eye-movement processing. In the temporal domain it is part of a fast sequence of activated areas, occupying the medial surface of occipital and parietal lobes. This fast sequence may represent a dorso-medial stream in the human brain
that conveys information from the visual cortex to the parietal lobe, frontal eye fields and the premotor cortex and controls visually guided movements.
Because animals are still widely used models for human brain function, the question of interspecies differences in functional organisation of the visual cortex is fundamental. To confirm interspecies homologue, the histology, relative position, functional profile, retinotopy, and connections should be similar across species. My studies showed that this putative human V6 has similar functional markers as its monkey homologue, such as a bias towards the peripheral visual field, motion sensitivity and activation at short latency and connections with the dorso-medial stream areas. These results, in line with previous function and lesion studies, contribute to evidence that human homologue of monkey V6 is located in the posterior bank of parieto-occipital sulcus.
The fourth aim of my thesis was to study the effect of top-down modulation in visual processing. The results showed two examples of response modulation in hierarchically low-level visual areas. Both of these modulations arose from top-down signals related to
cognitive tasks or motor behaviour. However, these modulations probably represent different processes. One enhances the signal locally at the attended region and may increase the stimulus saliency whereas the other is related to more non-specific dorsal stream activation and may reflect motor processing or resetting signals that prepare visual cortex for change in the environment.
8. Acknowledgements
This work was carried out in Brain Reserch Unit of Low Temperature Laboratory and Advanced Magnetic Imaging Centre of Helsinki University of Technology (Aalto University from 1.1.2010) and it was financially supported by the Academy of Finland, the Finnish Gradute School of Neuroscience, Sigrid Juselius Foundation, Jenny and Antti Wihuri Foundation, Finnish Medical Foundation and Oskar Öflund Foundation. I am most grateful for all financial support and to the Director of Low Temperature Laboratory Professor Mikko Paalanen and the Director of Brain Research Unit Professor Riitta Hari for providing this excellent working environment.
I would like to thank my instructor Docent Simo Vanni for supervising and guiding my journey in vision science and for all the hard work he has done. Thanks to past and present members of the vision group especially to Dr. Linda Henriksson, Lauri Nurminen, and Jaana Simola for friendship and to Dr. Juha Silvanto for his help with the language issues. I thank Professor Riitta Hari for kind support and for teaching me to think and talk a little faster. I would like thank the co-authors of my publications: Professor Claudio Galletti, Dr. Patrizia Fattori, Professor Riitta Hari, Dr. Lauri Parkkonen, Jaana Simola, Veronika von Pföstl, Dr.
Kimmo Uutela, and Docent Simo Vanni for the opportunity to work with you in fruitful collaborations. In addition, I wish to thank the preliminary examinators and the members of the follow-up group Dr. Iiro Jääskeläinen, Docent Jyrki Mäkelä, and Professor Turgut Tatlisumak for their effort and comments.
I want to express my deepest thanks to Marita Kattelus for friendly company and help with the measurements and Dr. Antti Tarkiainen for his patience and help with the computer matters. I thank the administrative forces of the Low Temperature Laboratory for helping me with many practical issues, and Helge Kainulainen and Markku Korhonen for technical support.
I spent many many years of my life working for my PhD and I want to thank people who made these years so funny and memorable. Thank you Maarit Aro, Dr. Gina Caetano, Liisa Helle, Jaana Hiltunen, Lotta Hirvenkari, Dr. Yevhen Hlushchuk, Annika Hultén, Dr. Jan Kujala, Miiu Kujala, Hannu Laaksonen, Satu Lamminmäki, Mia Liljeström, Dr. Lauri Parkkonen, Dr. Tiina Parviainen, Dr. Tommi Raij, Dr. Tuukka Raij, Pavan Ramkumar, Dr.
Hanna Renvall, Dr. Ville Renvall, Dr. Mika Seppä, Dr. Topi Tanskanen, Johanna Vartiainen,
Dr. Nuutti Vartiainen, and all others I forgot to mention. Special thanks to Sanna Malinen, with whom I shared the office and many joys, sorrows, and jokes.
Thanks to my parents Anu and Nisse for support, my late grandmother Telma for her enthusiasim and interest towards my work, and my dear old friends Mannis, Elina, Veera, Katri, Tuure, Juri, Jone, Vappu, and Elina for great company. Finally I want to thank my beloved family, my husband Jaska for his endless love and loyalty and our little Taru for being so lovely and perfect.
Helsinki, April 2010 Linda Stenbacka
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