A Developmental Model of Hemispheric Asymmetry of Spatial Frequencies

A Developmental Model of Hemispheric Asymmetries of Spatial Frequencies Ben Cipollini (bcipolli@ucsd.edu) Department of Cognitive Science, 9500 Gilman Dr., MC 0515, La Jolla, CA 92093 Garrison W. Cottrell (gary@ucsd.edu) Computer Science and Engineering, 9500 Gilman Dr., MC 0404, La Jolla, CA 92093 Abstract reading, face perception, and general mechanisms that may lead to other lateralized functions. Like lateralization, development is also key to understand- ing human cognition. Human development differs from that of any other primate (Martin, 1983; D. Geschwind & Rakic, 2013), including extinct homo species such as Neanderthal (Gunz, Neubauer, Maureille, & Hublin, 2010). Developmen- tal disorders come with a wide variety of cognitive impair- ments, including many involving atypical patterns of lateral- ization and inter-hemispheric transfer. How do development and learning interact with hemi- spheric lateralization of visual processing? Several hypothe- ses exist. A few are based on data showing that the right hemisphere develops earlier than the left (N. Geschwind & Galaburda, 1985; Hellige, 1993). As Hellige (1993) noted, during that time, the retina is also developing, during which acuity changes from predominantly LSF ranges to adult-like levels. Howard and Reggia (2007) theorized that during this period, magnocellular afferents to visual cortex enervate V2 in the RH, while later-developing parvocellular afferents in- nervate V2 in the LH to a greater extent, leading to lateral- ization of spatial frequency processing. Other approaches ex- ist; Plaut and Behrmann (2011) showed that anatomical con- straints on wiring length, the differential projection onto the retina of words (central) and faces (peripheral), and the left lateralization of language could lead to lateralization of faces to the RH (Fusiform Face Area) and words to the LH (Visual Word Form Area). In this paper, we show that the hypothesized asymmetry that leads to lateralization can emerge from a plausible inter- action between the asymmetric timing of connection pruning and visual acuity changes. We show this in a biologically plausible model under “natural image” experience and with cortical distortions known to exist in retinotopic visual areas. Then, in order to compare the results of our developmental model to our previous work, we also implemented a more bi- ologically plausible version of our model, also using “natural image” experience and the same cortical distortions. Lateralization touches virtually every function we think makes us human and interacts fundamentally with development. Here we connect lateralized function to anatomical asymmetries, and connect those anatomical asymmetries to temporal asym- metries in development. Our differential encoding (DE) model (Cipollini, Hsiao, & Cottrell, 2012; Hsiao, Cipollini, & Cottrell, 2013; Hsiao, Shah- bazi, & Cottrell, 2008) shows that lateralization in visual pro- cessing of spatial frequencies can be explained by a postu- lated asymmetry in the spatial spread of connections within retinotopic visual cortex. Here, we present three new mod- eling results supporting our previous conclusions. First, we show that our model results persist when trained on natural images, warped to match physical distortions of V1, showing that greater biological realism does not diminish our results. Second, we show that the hypothesized anatomical asymme- try can emerge from normal development, due to 1) the known temporal asymmetry in developmental pruning, coupled with 2) known acuity changes. This results in the two hemispheres being trained with images of different spatial frequency con- tent. Third, results from this developmental model suggest that the LH is not specialized for HSF processing; rather, the RH is specialized for LSF processing to the detriment of HSF pro- cessing. Keywords: Lateralization, local/global, spatial frequency, de- velopment, double filtering by frequency, differential encod- ing, visual processing, hemispheric asymmetry Introduction Lateralization is an essential part of virtually every function that we believe makes us human. Speaking, fine motor skills, spatial reasoning, emotion, reading, and face perception are all functions with an uneven representation across most in- dividual’s cortical hemispheres, but with a consistent hemi- spheric distribution across the human population. Lateralization of visual processing, in particular, has long been established (see Ivry and Robertson (1998) for a re- view). Subjects tend to respond more quickly and accu- rately to task-relevant low spatial frequency (LSF) informa- tion when it is presented to the left visual field (LVF, which the right hemisphere (RH) has preferred access to) vs. the right visual field (RVF, which the left hemisphere (LH) has preferred access to). The opposite holds for task-relevant high spatial frequency (HSF) information. These results fit nicely with LH lateralization for word reading (a HSF task) and RH lateralization for face perception (a task using con- figural information found in LSFs). The more general infer- ence is generally that the RH is specialized for LSF process- ing, while the LH is specialized for HSF processing. We be- lieve that understanding mechanisms behind lateralization of spatial frequency (SF) processing may give insight into word The Differential Encoding (DE) Model Our approach and model of lateralization of visual processing was initially a response to the Double Filtering by Frequency (DFF) model by Ivry and Robertson (1998). Following the lead of Sergent (1982), they argued that the hemispheres are generically lateralized for SF processing across modalities, and proposed that lateralization of spatial frequency process- ing plays a causal role in the local/global effects in hierar-