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Area TEO and “Area ?”: cytoarchitectonic confusion corrected by connectivity and cortical ablation

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Abstract

Throughout history, researchers who examine the structure and function of the brain debate one another about how cortical areas are defined, as well as how these areas should be named. Different pieces of empirical evidence are used to define brain areas and it is important to preserve the accurate history of this evidence and the timeline of studies that lead to areal definitions that are either still used today or have been modified. As such, this paper traces the early history of a brain area located at the junction between the occipital and temporal lobes of the macaque known as TEO. This historical analysis leads to four main findings. First, even though Bonin and Bailey are credited with the definition of area TEO in 1947, they did not have the cytoarchitectonic evidence to support the distinction of TEO from adjacent areas. Second, the first evidence definitively separating area TEO from TE was actually based on connectivity as identified with strychnine neuronography by Petr et al. in 1949. Third, causal evidence from ablation studies conducted by Iwai and Mishkin (Experimental Neurology 25(4):585–594, 1969) supported this distinction by showing that TEO and TE were functionally distinct from one another. Fourth, researchers in the 1970s began referring to TEO as posterior inferotemporal (PIT) and TE as anterior inferotemporal (AIT), which is an important historical clarification as the PIT/AIT nomenclature is presently attributed to studies conducted more than a decade later. Altogether, this paper aims to preserve the historical origin of area TEO, as well as the empirical evidence that was used to originally differentiate this cortical expanse from surrounding areas.

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Notes

  1. During the time periods discussed in the present paper, pioneering brain research was being conducted with different types of methods. However, the focus of the present paper is on the studies of cortical ablation and strychnine neuronography as they are critical historically for the original distinction among areas TE, TEO, and OA. Pioneering neurophysiology studies of TE and TEO (Gross et al. 1969, 1972; Boussaoud et al. 1991; and many others) were also being conducted during the time periods discussed in the present paper, but discussion of these studies is beyond the scope of the present review. I should also clarify that particular attention is placed on studies conducted by Iwai et al. as many of them are conference proceedings that remain in the stacks of libraries. As such, they are largely excluded from the modern literature, but are integral for the historical origin of TEO.

  2. If such a description does exist in the literature and I have missed it, I am hopeful that a reader would contact me or write a letter to the journal (or both) to assure that the history of TEO is preserved.

  3. Initially, it was unclear as to why Bonin and Bailey cited Economo (1929) consistently throughout their monograph instead of the original Economo and Koskinas (1925) atlas that was published four years prior. But, in a paper published by Peden and Bonin (1947) in the same year as the Bonin and Bailey monograph, a footnote revealed that the reason was because of availability. Peden and Bonin write: “We prefer to cite Economo’s English summary since it is more readily available than the costly cytoarchitectural atlas published with Koskinas in 1925.” Peden and Bonin (1947), pg. 40.

  4. Consistent with this idea, Triarhou (2007b) refers to area PHP as the “Basal (temporooccipital) parietal area at parietal entrance,” area PHT as the “Basal (temporooccipital) parietal area at temporal entrance,” and PHO as the “Basal (temporooccipital) parietal area at occipital entrance” (Triarhou 2007b, Table 2, pg. 208).

  5. Interestingly, while Bonin and Bailey did not include TEO in the frontispiece of their 1947 monograph of the macaque brain, they did include area PH on the frontispiece of their 1950 monograph (with McCulloch) of the chimpanzee brain.

  6. Cowey and Gross (1970) included a footnote in their paper with similar concerns. They write: “The terminology for the subdivisions of the non-striate visual areas of the occipital and temporal lobes of the monkey is still rather confusing. This is hardly surprising, for the subdivision of these areas on cytoarchitectonic grounds by different authorities is contradictory and the study of the properties of single units in these areas has only begun. Although the recent demonstrations by Zeki (1969) and Cragg and Ainsworth (1969) that lateral striate cortex has two topographic and a third non-topographic projection onto prestriate cortex is a major step forward, the exact boundaries of these projections and their detailed relations to the various cytoarchitectonic subdivisions and subdivisions based on electrophysiological data are not yet entirely clear. Since the terminology used in behavioral studies of lesions of the non-striate visual areas is also inconsistent, it may be helpful to explain the terminology we have used in this report. We have called our posterior lesions “foveal prestriate lesions” because they include the entire area of prestriate cortex to which foveal striate cortex selectively projects (Zeki 1969; Cragg and Ainsworth 1969). Simply to call them prestriate cortex lesions or posterior inferotemporal cortex lesions is misleading because they include far less than the former and far more than the latter. Our inferotemporal lesions correspond closely to Von Bonin and Bailey’s “Area TE”. However, numerous publications on the behavioral effects of removing “inferotemporal” cortex illustrate lesions which often extend posterior to “Area TE” as far as the inferior occipital sulcus and thus may include part of foveal prestriate cortex. We therefore wish to stress that our inferotemporal lesions are restricted to area TE and may not be comparable to some “inferotemporal” lesions in other studies.” Cowey and Gross (1970), Pgs. 128–129.

  7. Table 1 included in the present manuscript is reproduced from Table 1 from Iwai (1978).

  8. Though Zeki (1996) cites Felleman and Van Essen (1991) for the definition of PIT, Van Essen and colleagues re-proposed the definition and name of PITd and PITv in a different paper the year prior (Van Essen et al. 1990) in which they write: “The fact that there are two pairs of topographically organized foci suggests that they form two distinct areas, which we have termed PITd and PITv (dorsal and ventral subdivisions of the posterior inferotempo-ral area).” Van Essen et al. (1990, pg. 688).

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Acknowledgements

I thank Mona Rosenke for comments on a previous version of this manuscript.

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This research was funded by NEI Grant 1 RO1 EY 02391501A1 and start-up funds provided by UC Berkeley.

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  1. Department of Psychology, University of California, Berkeley, Berkeley, CA, 94720, USA

    Kevin S. Weiner

  2. Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA

    Kevin S. Weiner

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Weiner, K.S. Area TEO and “Area ?”: cytoarchitectonic confusion corrected by connectivity and cortical ablation. Brain Struct Funct 223, 3515–3529 (2018). https://doi.org/10.1007/s00429-018-1714-1

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