Functional architecture in monkey inferotemporal cortex revealed by in vivo optical imaging
Introduction
The ventral visual cortical pathway, which interconnects the striate, prestriate, and inferotemporal areas, is critical for the visual identification of objects (Gross, 1973, Dean, 1976, Mishkin et al., 1983). The anterior part of the inferotemporal cortex, defined as cytoarchitechtonic area TE, is the last exclusively visual area along the pathway. TE cells selectively respond to object attributes such as shape, color, texture or a combination of these (Gross et al., 1972, Desimone et al., 1984, Tanaka et al., 1991, Komatsu and Ideura, 1993, Kobatake and Tanaka, 1994, Sheinberg and Logothetis, 1997). The object features to which TE cells selectively respond are more complex than the features to which cells in the earlier stages respond (Gallant et al., 1993, Kobatake and Tanaka, 1994, Gallant et al., 1996). The size of the receptive fields increases towards TE along the ventral visual cortical pathway (Gattass et al., 1988, Boussaoud et al., 1991, Kobatake and Tanaka, 1994).
Based on single-cell recordings, Fujita et al. (1992) proposed that TE cells responsive to similar object features cluster vertically across the cortical layers to form a column. The width of individual columns was estimated to be ∼0.4 mm. To confirm the existence of such clustering of cells, and if present, to further study the spatial organization of the clustering, optical imaging based on intrinsic signals was carried out in the monkey area TE in the present study.
The optical imaging has been successfully used in the studies of the functional organization in V1, V2, MT, and more recently TE and V4 (Grinvald et al., 1988, Frostig et al., 1990, Ts’o et al., 1990, Bonhoeffer and Grinvald, 1991, Blasdel, 1992, Malonek et al., 1994, Wang et al., 1996, Ghose and Ts’o, 1997), and was shown to be superior to single-cell recordings for studying the functional organization. In optical imaging the local average of neuronal activities is measured simultaneously over a wide cortical region, whereas such measurement is difficult with single-cell recordings.
Section snippets
Materials and methods
Five adult Japanese monkeys (Macaca fuscata) were prepared for repeated experiments. The optical imaging was conducted in the dorsolateral part of TE (Fig. 1(A)) in eight hemispheres. Both hemispheres were used in succession in three of the five monkeys. For two of the eight hemispheres, single-cell recordings with microelectrodes were first conducted in several separate sessions to determine the visual stimuli effective for activation of the TE region to be subjected to the optical imaging,
Results
Data described here are based on the recordings from eight hemispheres of five monkeys. Ninety three successful images were obtained for moderately complex non-face features including the critical features, 63 for faces, and seven for simple control stimuli, besides many control images obtained without visual stimulation.
Discussion
The visual stimuli evoked two kinds of optical signals, global darkening and localized spots, in the present study. Previous studies have shown that the intrinsic optical signals measured around 600 nm mainly reflect the concentration of deoxygenated hemoglobin in capillaries (Frostig et al., 1990, Malonek and Grinvald, 1996), which in turn reflects the average level of synaptic activity in the particular area (Das and Gilbert, 1995). Because: (1) the global darkening covered more than 90% of
Acknowledgements
This study was supported by the Frontier Research Program/RIKEN, Brain Foundation/Kowa Life Science Foundation, and Brain Science Foundation.
References (35)
- et al.
Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey
Brain Res.
(1985) - et al.
Shape representation in the inferior temporal cortex of monkeys
Curr. Biol.
(1995) - et al.
Object vision and spatial vision: two cortical pathways
Trends Neurosci.
(1983) - et al.
A tandem-lens epifluorescence macroscope, hundred-fold brightness advantage for wide-field imaging
J. Neurosci. Methods
(1991) - American Association for the Advancement of Science, 1996. Science 272,...
Orientation selectivity, preference, and continuity in monkey striate cortex
J. Neurosci.
(1992)- et al.
Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns
Nature
(1991) - et al.
Visual topography of area TEO in the macaque
J. Comp. Neurol.
(1991) - et al.
Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex
Nature
(1995) Effects of inferotemporal lesions on the behavior of monkeys
Psychol. Bull.
(1976)
Stimulus-selective properties of inferior temporal neurons in the macaque
J. Neurosci.
Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals
Proc. Natl. Acad. Sci. USA
Columns for visual features of objects in monkey inferotemporal cortex
Nature
Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex
Science
Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey
J. Neurophysiol.
Visuotopic organization and extent of V3 and V4 of the macaque
J. Neurosci.
Form processing modules in primate area V4
J. Neurophysiol.
Cited by (126)
Early Emergence of Solid Shape Coding in Natural and Deep Network Vision
2021, Current BiologyReversible Inactivation of Different Millimeter-Scale Regions of Primate IT Results in Different Patterns of Core Object Recognition Deficits
2019, NeuronCitation Excerpt :Taken together these results demonstrate the necessity of the IT cortex for a wide range of general core object recognition behaviors and reveal that—even outside of face patches—the IT cortex has behaviorally critical topographic organization of visual features. These findings are consistent with and suggested by prior physiology work (Wang et al., 1998; Tsunoda et al., 2001; Kreiman et al., 2006 for sub-millimeter columnar organization; Lafer-Sousa and Conway, 2013; Conway, 2018 for broad spatial organization of IT), but, to our knowledge, this is the first demonstration of a topographically organized causal role of IT in general core object recognition. Additionally, we tested whether the deficits were evenly distributed over the five objects across all inactivation sites.
Electrophysiological evidence for separation between human face and non-face object processing only in the right hemisphere
2015, International Journal of PsychophysiologyInsights into cortical mechanisms of behavior from microstimulation experiments
2013, Progress in Neurobiology