First-order analysis of optical flow in monkey brain.

Abstract

Optical flow is a rich source of information about the three-dimensional motion and structure of the visual environment. Little is known of how the brain derives this information. One possibility is that it analyzes first-order elementary components of optical flow, such as expansion, rotation, and shear. Using a combination of physiological recordings and modeling techniques, we investigated the contribution of the middle superior temporal area (MST), a third-order cortical area in the dorsal visual pathway that receives inputs from the medial temporal area (MT Optical flow, which can be defined as the apparent motion of the image brightness on the retina, has long been considered as a useful representation of visual motion information (1). According to a fundamental theorem of kinematics, or Helmholtz theorem (2), optical flow, within a small area of the visual field, can be seen as the sum of a translation with four elementary flow components (EFCs): a rotation (circular motion), an expansion (radial motion), and two components of shear (deformations) (3). This result has been successfully used in computer and computational vision for the analysis of motion (3-7). In addition, EFCs have been shown to be biologically relevant (8,9). Therefore, as suggested by recent studies in which middle superior temporal area (MST) cells of the monkey brain were reported to be selective for rotation and expansion (10-15), one may propose that the brain explicitly represents EFCs. MST is a third-order cortical area in the dorsal pathway leading to the parietal cortex (16). It receives inputs from the middle temporal area (MT) (17, 18), which has been implicated in motion analysis (19)(20)(21)(22), and is mainly driven by magnocellular input (23). However, there is disagreement about the degree of selectivity of MST cells: MST cells have been reported to be selective for a single EFC (10, 24) but also for several components (12, 13). Furthermore, there is no information about whether or not complex motion patterns are decomposed into the (linear) superposition of EFCs. Finally, it is not clear how the MST selectivity for EFCs is generated.Therefore, we quantitatively compared responses of cortical cells to translation and EFCs in both areas (MST and MT). To clearly distinguish between responses to local flow vectors and to global arrangements of vectors characteristic of EFCs, we systematically tested for the position invariance of the selectivity. Once selectivity for an EFC was established, we then studied the responses of MST cells to a combination of components, keeping one component constant. The results of the physiological study were used to model the transformations effected by the MST cells on MT input. METHODSWe have recorded from single MST and MT neurons of anesthetized and paralyzed monkeys (Macaca fascicularis) to obtain stable recordings over several hours and precisely localize the recorded units with respect to area and layer. The monkeys were anesthetized with sufentanil (5 pg-kg-1lh-1) and paralyze...

Translation Speed Compensation in the Dorsal Aspect of the Medial Superior Temporal Area

“…The neurons were first tested for their optic flow preferences as well as for preferred pursuit direction. Consistent with previous studies, we found that MSTd neurons are selective to spiral space patterns, especially for those that have an expansion component (Saito et al, 1986;Duffy and Wurtz, 1991a,b;Orban et al, 1992;Graziano et al, 1994;Sakata et al, 1994). The majority of neurons in MSTd show significant tuning to laminar motion; however, we did not find a contralateral visual motion bias that others have reported (Komatsu and Wurtz, 1988a;Shenoy et al, 2002).…”

Multimodal Representation of Space in the Posterior Parietal Cortex and Its Use in Planning Movements

“…Also, optic flow patterns generated during self-motion often contain significant rotation. Since MSTd expansion cells respond poorly to rotation (Orban et al 1992, Graziano et al 1994, rotation cells might be required in some cases to provide information about heading. If so, they would have to correct for pursuit eye movements by shifting their receptive fields orthogonally to the pursuit direction, as in fact they do.…”

Representation of Head-Centric Flow in the Human Motion Complex

“…MT neurons have relatively small receptive fields and carry purely visual signals that encode the basic elements of motion. Neurons in MST, conversely, have large receptive fields that prefer certain patterns of visual motion (Duffy and Wurtz, 1991;Orban et al, 1992;Graziano et al, 1994;Lappe et al, 1996), and their responses are often modulated by eye position (Bremmer et al, 1997), eye velocity (Bradley et al, 1996;Page and Duffy, 1999), and vestibular signals (Shenoy et al, 1999). This integration of visual and nonvisual signals in MST could make it a crucial area for the perception of self-motion (Britten and van Wezel, 1998;Page and Duffy, 2003).…”