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Segregation Within Afferent Pathways in Primate Vision Sujata Roy March Segregation Within Afferent Pathways in Primate Vision Sujata Roy Submitted in total fulfillment of the requirements of the degree of Doctor of Philosophy March 2009 Department of Optometry & Vision Sciences The University of Melbourne Abstract The current knowledge of the visual pathways in primates includes the patterns of projection from the retina through the dorsal lateral geniculate nucleus (dLGN) to the striate cortex (V1) and the extra-striate projections towards the dorsal and ventral streams. Cells with short wavelength sensi- tive cone (S-cone) inputs in the dLGN have been studied extensively in New World marmosets but not in Old World macaques. This thesis presents re- sults from studies in the macaque monkey which are more relevant to humans since humans are closer in evolution to Old World than New World monkeys. The spatial, temporal, chromatic and orientation preferences of neurons in the dLGN of the macaque were investigated by electrophysiological meth- ods. The physiological findings of cells with S-cone inputs were compared to cells with opponent inputs from the long and medium wavelength sensitive cones (L-cones & M-cones, respectively). The cells receiving S-cone inputs (blue-yellow or B-Y cells) preferred lower spatial frequencies than the cells with opponent L-cone and M-cone inputs (red-green or R-G cells). Ortho- dromic latencies from optic chiasm stimulation were measured where possible to distinguish differences in conduction velocity between the cell groups. Al- though the B-Y cells usually had longer latencies than R-G cells, there was considerable overlap between the cell groups. The recorded cells were localised through histological reconstruction of dLGN sections stained for Nissl substance. The distribution of B-Y cells within the dLGN was compared to the distribution of R-G cells. The majority of B-Y cells were located within the intercalated koniocellular layers as well as the koniocellular bridges (extensions of the koniocellular layers into the adjacent parvocellular layers). The B-Y cells were also largely segregated within the middle dLGN layers (K3, P3, K4 & P4). The R-G cells were i mainly concentrated within the parvocellular layers (P3, P4, P5 & P6) and were evenly distributed throughout the middle and outer layers of the dLGN. The study also included recordings from the extra-striate middle tem- poral area (MT) to determine whether a fast S-cone input exists from the dLGN to area MT which bypasses V1. The pattern of cone inputs to area MT neurons was investigated before and during inactivation of V1. The in- activation was done through reversible cooling with a Peltier thermocouple device or focal inactivation with γ-amino butyric acid (GABA) iontophore- sis. Precise inactivation of V1 to the topographically matching visual fields of the recording sites in area MT revealed a preservation of all three cone inputs in many cells. The subcortical sources of these preserved inputs are discussed with their relevance to blindsight, which is the limited retention of visual perception after V1 damage. Analysis of the latencies of area MT cells revealed a rough segregation into latencies faster or slower than 70 ms. Cells both with and without a significant change in response during V1 inactiva- tion were present in each group. The findings reported in this thesis indicate that some of the preserved inputs in area MT during V1 inactivation may be carried by a direct input from the dLGN which bypasses V1. ii Declaration This is to certify that: 1. The thesis comprises only my original work toward the PhD except where indicated in the Preface; 2. Due acknowledgment has been made in the text to all other material used; 3. The thesis is less than 100,000 words in length, exclusive of words in tables, figures, bibliographies and appendices. Sujata Roy iii this page has been left blank intentionally iv Preface Some of the results described in this thesis have appeared in the following publications and abstracts: Publications: Roy, S., Saalmann, Y.B., Jayakumar, J., Hu, D., Martin, P., Dreher, B., Vidyasagar, T.R. (2009). Segregation of S-cone inputs within the macaque dorsal lateral geniculate nucleus. Submitted for peer review to the European Journal of Neuroscience; on 19th February, 2009. Abstracts: Roy, S., Saalmann, Y.B., Jayakumar, J., Hu, D., Martin, P., Dreher, B., Vidyasagar, T.R. (2007). Laminar segregation of cell types in the dor- sal lateral geniculate nucleus of the macaque monkey. International Brain Research Organisation (IBRO) Conference in conjunction with Australian Neuroscience Society (ANS) Annual Meeting, Melbourne 2007. Roy, S., Saalmann, Y.B., Jayakumar, J., Hu, D., Martin, P., Dreher, B., Vidyasagar, T.R. (2007). Laminar segregation of blue-yellow cells in the dorsal lateral geniculate nucleus of the macaque monkey. Vision Down Under Symposium, Satellite Vision Seminars for IBRO, Cairns 2007. v this page has been left blank intentionally vi Acknowledgments Thanks to Professor Vidyasagar, Professor Martin, to the lab members and all the people involved in the experiments for help with data collection and analysis - Yuri, Jai, Peter, Pinate, Uli, Brett, Patricia, and to Josephine for her friendship. The project was supported by the Australian National Health and Med- ical Research Council. The use of the facilities at the Department of Op- tometry and Vision Sciences at the University of Melbourne were essential to this study. Thanks to Professor Martin for generous sharing of the re- sources at the National Vision Research Institute. My efforts were aided by financial support from the Faculty of Science Scholarship at the University of Melbourne. I am grateful to my mum and dad for their frequent visits and encour- aging me every step of the way, my sister for inspiring me with her musical talents. Also to my friends during my time in Melbourne thanks for the good company. I remain indebted to Dom for his hours of proof reading, his constructive criticism which greatly helped me improve my writing skills and his helpful advice on every aspect of the thesis, as well as life in general! vii this page has been left blank intentionally viii Contents 1 Introduction 1 1.1 Background . 1 1.2 Aims of the thesis . 4 1.3 Chapter outline . 5 2 The Visual Pathways 11 2.1 Old World and New World Primates . 11 2.2 Overview of the Visual Pathways . 13 2.3 Retinal ganglion cells . 14 2.4 The dLGN . 20 2.5 The Koniocellular Pathway . 25 2.6 The Visual Cortex . 35 2.7 The Middle Temporal area (MT) . 42 3 Experimental Methods 51 3.1 Experimental Animals . 51 3.2 Anaesthesia and Surgery . 52 3.3 dLGN Recordings . 53 3.4 Optics and Visual Stimuli . 54 3.5 Electrophysiological data . 63 3.5.1 Receptive field dimensions . 63 3.5.2 Non-linearity Index . 64 ix 3.5.3 Low Frequency Ratio (LFR) . 65 3.5.4 Temporal Frequency Ratio (TFR)............ 65 3.5.5 Contrast gain (Rm/b)................... 66 3.5.6 Orientation and Direction Selectivity . 67 3.5.7 Orthodromic latencies . 69 3.5.8 Statistical tests . 70 3.6 Area MT recordings . 71 3.6.1 Inactivation of the visual cortex . 71 3.6.2 Aperture size . 75 3.6.3 Stimulus characteristics . 75 3.7 Iontophoretic Inactivation using GABA . 78 3.8 Histological processing . 80 4 Physiological properties of S-cone input cells in the dLGN 83 4.1 Introduction . 83 4.2 Methods . 88 4.3 Results . 93 4.3.1 Spatial frequency . 93 4.3.2 Luminance artifacts . 96 4.3.3 Receptive field dimensions . 98 4.3.4 Non-linearity index . 102 4.3.5 Low Frequency Ratio . 103 4.3.6 Temporal Frequency Ratio . 104 4.3.7 Contrast gain . 106 4.3.8 Orientation preference & Direction selectivity . 107 4.3.9 Orthodromic latencies . 110 4.4 Discussion . 112 5 Laminar distribution of S-cone input cells in the dLGN 117 5.1 Introduction . 117 x 5.2 Methods . 122 5.3 Results . 126 5.3.1 Koniocellular bridges . 126 5.3.2 Laminar distribution of cells . 127 5.4 Discussion . 133 6 Responses in area MT with cortical inactivation 139 6.1 Introduction . 139 6.2 Methods . 144 6.3 Results . 149 6.3.1 General findings . 149 6.3.2 Eccentricities . 149 6.3.3 Methods of Inactivation . 152 6.3.4 Responses to different cone modulating stimuli . 154 6.3.5 Response ratios with changing eccentricity . 161 6.3.6 Latencies of area MT cells with V1 cooling . 166 6.4 Discussion . 179 7 Summary & Conclusions 187 xi this page has been left blank intentionally xii List of Figures 2.1 Organisation of a cell’s receptive field . 15 2.2 Connections of the S-cone On pathway . 18 2.3 Cross-section of the macaque dLGN . 21 2.4 The topographic organisation of the dLGN . 22 2.5 Distribution of koniocellular neurons within the dLGN . 28 2.6 Termination patterns of dLGN afferents within V1 . 37 2.7 Segregation of inputs to the main termination layer 4C of V1 . 38 2.8 Areas of the dorsal and ventral visual streams . 43 2.9 Inputs to area MT from various locations . 46 3.1 Azimuth and elevation for the stimuli . 60 3.2 Responses quantified by the vector size and direction . 61 3.3 Responses to chromatic modulation for four cell types . 62 3.4 Determination of the low frequency ratio (LFR) . 65 3.5 Determination of the temporal frequency ratio (TFR) . 66 3.6 Quantifying contrast gain for the cells . 67 3.7 Determination of the Orientation Index . 68 3.8 Location of electrodes for orthodromic latency measurements . 70 3.9 Visual representation of the cortex with adjacent visual areas .
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