The project goal is to explore the relationship between experience, expertise, and modular organization in the temporal lobe. During the last 4 years this laboratory has explored the functional anatomy and mechanisms of face detection and recognition, and the present proposal is to extend these studies to simple shapes and to the role of intensive early experience in generating anatomically distinct functionally specialized domains. There are distinct regions of the brain, reproducible from one person to the next, specialized for processing the most universal forms of human expertise;e.g., face processing, speech processing, and reading. Face-selective regions in the temporal lobe have been identified using functional magnetic resonance imaging (fMRI) in both humans and macaques, and in humans visual recognition of letters and words is also localized, to the same part of the temporal lobe, but more lateral and posterior and in the opposite hemisphere. Because of the importance of social interactions in primates, one could imagine a face-specific region being generated by natural selection, but it is unlikely that a cortical region specific for written words could have evolved, given that humans have been using written language for only a few thousand years, and literacy has been widespread for at most a few hundred years. The fact that most people have intensive early experience with both faces and symbols prompted the question of whether intensive early experience could cause monkeys to develop anatomical specializations for processing stimuli they never naturally use. After intensive training, juvenile monkeys learned symbols faster than adult monkeys and developed more "fluency" in responding to them. Furthermore fMRI revealed that juveniles, but not adults, develop regions in their temporal lobes selectively responsive to the learned symbols, but not to visually similar but unfamiliar symbols. This provides the unique opportunity to study the physiology and functional organization of a training-induced cortical module selective for simple shapes not normally experienced by monkeys, and to compare this region to the same cortical region in untrained and late-trained animals. Single-unit electrophysiology and fMRI will be used in parallel and in conjunction to explore the functional specialization in these training-induced symbol recognition regions and to explore the differences in the same parts of the temporal lobe in early versus late trained animals. Differences in response properties in this region between untrained, late trained, and early trained animals will illuminate how experience interacts with maturational gradients during development. The learned symbols are simple shapes, with simple features shared among the learned symbol set, therefore single unit physiology should reveal how training affects the way shape selective cells combine simple features to generate more complex shape selectivity. The proposed study should lead to a deeper understanding of how early social and educational experience or deprivation affects the developing brain.

Public Health Relevance

The goal of the proposed research is to gain a deeper understanding of the importance and irreversibility of early social and educational experience and deprivation by providing a mechanistic understanding of how intensive early experience can modify the modular organization of the brain, and lead to the expert fluent processing characteristic skills like face recognition, language, and reading. The implications for mental health are enormous: if intensive early social experience is necessary to develop functional segregation of face processing, and if functional segregation is necessary for proficient face processing, then the timing and quantity of early social experience may be critical in the etiology and/or remediation of autism spectrum disorders. Early life experiences clearly can have long lasting consequences, and we need to better understand how the timing of some kinds of experience, or the lack thereof, can permanently change how the brain processes corresponding kinds of information.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY016187-07
Application #
8322602
Study Section
Cognitive Neuroscience Study Section (COG)
Program Officer
Steinmetz, Michael A
Project Start
2004-12-01
Project End
2016-06-30
Budget Start
2012-07-01
Budget End
2013-06-30
Support Year
7
Fiscal Year
2012
Total Cost
$537,202
Indirect Cost
$218,202
Name
Harvard University
Department
Biology
Type
Schools of Medicine
DUNS #
047006379
City
Boston
State
MA
Country
United States
Zip Code
02115
Livingstone, Margaret S; Pettine, Warren W; Srihasam, Krishna et al. (2014) Symbol addition by monkeys provides evidence for normalized quantity coding. Proc Natl Acad Sci U S A 111:6822-7
Srihasam, Krishna; Mandeville, Joseph B; Morocz, Istvan A et al. (2012) Behavioral and anatomical consequences of early versus late symbol training in macaques. Neuron 73:608-19
Livingstone, Margaret S; Lafer-Sousa, Rosa; Conway, Bevil R (2011) Stereopsis and artistic talent: poor stereopsis among art students and established artists. Psychol Sci 22:336-8
Libedinsky, Camilo; Livingstone, Margaret (2011) Role of prefrontal cortex in conscious visual perception. J Neurosci 31:64-9
Livingstone, Margaret S; Srihasam, Krishna; Morocz, Istvan A (2010) The benefit of symbols: monkeys show linear, human-like, accuracy when using symbols to represent scalar value. Anim Cogn 13:711-9
Srihasam, Krishna; Sullivan, Kevin; Savage, Tristram et al. (2010) Noninvasive functional MRI in alert monkeys. Neuroimage 51:267-73
Chen, Haiwen; Russell, Richard; Nakayama, Ken et al. (2010) Crossing the 'uncanny valley': adaptation to cartoon faces can influence perception of human faces. Perception 39:378-86
Freiwald, Winrich A; Tsao, Doris Y; Livingstone, Margaret S (2009) A face feature space in the macaque temporal lobe. Nat Neurosci 12:1187-96
Howe, Piers D; Horowitz, Todd S; Morocz, Istvan Akos et al. (2009) Using fMRI to distinguish components of the multiple object tracking task. J Vis 9:10.1-11
Libedinsky, Camilo; Savage, Tristram; Livingstone, Margaret (2009) Perceptual and physiological evidence for a role for early visual areas in motion-induced blindness. J Vis 9:14.1-10

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