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Electronic Letters to:

BehavioralSystemsCognitive:
David A. Crowe, Bruno B. Averbeck, and Matthew V. Chafee
Neural Ensemble Decoding Reveals a Correlate of Viewer- to Object-Centered Spatial Transformation in Monkey Parietal Cortex
J. Neurosci. 2008; 28: 5218-5228 [Abstract] [Full text] [PDF]
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[Read eLetter] Transformations in 7a: challenging 'vision for action' or bridging the dorsal and ventral streams?
Lee H de-Wit, Cristiana Cavina-Pratesi   (18 July 2008)

Transformations in 7a: challenging 'vision for action' or bridging the dorsal and ventral streams? 18 July 2008
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Lee H de-Wit,
Graduate Student
Department of Psychology, Durham University, DH1 3LE,
Cristiana Cavina-Pratesi

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Re: Transformations in 7a: challenging 'vision for action' or bridging the dorsal and ventral streams?

l.h.de-wit{at}durham.ac.uk Lee H de-Wit, et al.

Crowe et al’s data are consistent with Ungerleider and Mishkin’s (1982) classical delineation between a cortical ventral stream that is engaged in identifying and recognizing objects and a dorsal stream that is concerned with computing spatial relationships. Milner and Goodale (1995) have challenged this conceptualization of the functional specialization of the dorsal and ventral streams. In doing so these authors question not only the forms of spatial encoding undertaken by the dorsal stream but, more critically, question the purpose for which that spatial encoding is employed. Within Ungerleider and Mishkin’s framework the dorsal stream underlies our conscious perception of spatial relationships. Milner and Goodale have argued that not only is scene-based spatial cognition the preserve of the ventral stream (Carey, Dijkerman, Murphy, Goodale, Milner, 2006) but that spatial coding in the dorsal stream does not serve perception per se. Rather, in conjunction with certain types of object- form analysis, the dorsal stream functions to supply information regarding ‘how’ to act upon objects in the world.

At first glance Crowe and colleagues’ results appear not only to support Ungerleider & Mishkin’s (1982) proposed division, but also seem to contradict Milner and Goodale’s model. Indeed, the task utilized by Crowe et al. is quite cunningly designed to avoid any need to program spatial relationships for making an action. The monkey does not, for example, have to respond by pointing to the left or right, but rather has to press abutton at the right point in time. Such a behavioral output, however, does not guarantee that the dorsal stream will not compute information to guide an action. In fact, several studies have shown that the dorsal stream performs computations related to performing a given action even if the participant does not intend to act on that information (Grezes, Tucker, Armony, Ellis and Passingham, 2003). Furthermore many area-7 neurones are clearly modulated by the execution of manual actions: whilst they might encode the properties of a stimulus viewed passively they will respond much more vigorously if the animal performs an action on that stimulus (Mountcastle et al., 1975).

Moreover, the form of object-centered spatial coding identified by Crowe and colleagues could play an important role in ‘vision for action’. When picking up a cup, for example, it is important to encode the location of the handle with respect to the overall object. There are, however, more complicated forms of spatial representation that would prove more difficult for the ‘vision for action’ model of the dorsal stream. Milner and Goodale argue that allocentric encoding (between different objects) requires the ventral stream (see Carey et al., 2006). Distinguishing between truly allocentric encoding and object-based encoding (between elements of a single object), of course, raises the issue of defining what is perceived as a single object. The inverted T-stimulus used by Crowe and colleagues intuitively groups to form a single object. It would therefore be theoretically important to extend the Crowe et al. paradigm to explore whether there are neurons in area 7a that encode not just the relationship of a target element to a single object but the relationship between objects, for example by locating them at distances at which they would clearly not be grouped into a single object. If activity in area 7a neurones still predicted the relationship between these objects, it would follow that the dorsal stream could encode complex spatial relationships that play no obvious role in action and provide a serious challenge to the vision-for-action model of the dorsal stream.

Finally, it is worth drawing attention to the interesting coincidence between the localization of the proposed viewer- to object-centered transformation and the location of 7a within the anatomical hierarchy that embodies the dorsal and ventral streams. Andersen et al. (1990) point out that although there are other connections between early levels of processing in the two streams, 7a provides the only direct link between the endpoints of processing within the two streams. Andersen and colleagues therefore suggest that area 7a may play a theoretically significant role in communicating information in the two streams. Milner and Goodale themselves argue that communication between the two streams is often required for coordinated behavior. For instance, the dorsal stream might program the exact kinematics of how to act upon a given object while the ventral stream selects which objects to act upon (Milner and Goodale, 1995).

In the context of communicating between different egocentric (i.e. hand-, head-, or retina-based) frames of reference purely within the parietal lobe, Cohen and Andersen (2002) have argued that the establishment of a common frame of reference could prove useful in coordinating the action of multiple effectors. The creation of an object- centered frame of reference in an area that just happens to provide the most direct connection between the higher levels of processing between the two streams might have an important role to play in establishing a common reference frame within which the two streams can communicate.

References:

Andersen RA, Asanuma C, Essick G, Siegel RM (1990) Corticocortical Connections of Anatomically and Physiologically Defined Subdivisions within the Inferior Parietal Lobule. J Comp Neurol, 296(1), 65-113.

Carey DP, Dijkerman HC, Murphy KJ, Goodale MA, Milner AD (2006) Pointing to places and spaces in a patient with visual form agnosia. Neuropsychologia 44(9): 1584-1594.

Cohen YE, Andersen RA (2002) A common reference frame for movement plans in the posterior parietal cortex. Nat Rev Neurosci 3(7):553-62

Grezes J, Tucker M, Armony JL, Ellis R, Passingham RE (2003) Objects automatically potentiate action: an fMRI study of implicit processing. Eur J Neurosci 17: 2735-2740.

Milner AD, Goodale MA, (1995) The Visual Brain in Action. Oxford: Oxford University Press.

Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior Parietal Association Cortex of Monkey - Command Functions for Operations within Extrapersonal Space. J Neurophysiol 38(4): 871-908.

Ungerleider LG, Mishkin M, (1982) Two cortical visual systems. In: Analysis of Visual Behavior (Ingle DJ, Goodale MA, Mansfield RJW, ed), pp549-586. Cambridge MA: MIT Press.

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