scholarly journals Escaping the nocturnal bottleneck, and the evolution of the dorsal and ventral streams of visual processing in primates

Author(s):  
Jon H. Kaas ◽  
Hui-Xin Qi ◽  
Iwona Stepniewska

Early mammals were small and nocturnal. Their visual systems had regressed and they had poor vision. After the extinction of the dinosaurs 66 mya, some but not all escaped the ‘nocturnal bottleneck’ by recovering high-acuity vision. By contrast, early primates escaped the bottleneck within the age of dinosaurs by having large forward-facing eyes and acute vision while remaining nocturnal. We propose that these primates differed from other mammals by changing the balance between two sources of visual information to cortex. Thus, cortical processing became less dependent on a relay of information from the superior colliculus (SC) to temporal cortex and more dependent on information distributed from primary visual cortex (V1). In addition, the two major classes of visual information from the retina became highly segregated into magnocellular (M cell) projections from V1 to the primate-specific temporal visual area (MT), and parvocellular-dominated projections to the dorsolateral visual area (DL or V4). The greatly expanded P cell inputs from V1 informed the ventral stream of cortical processing involving temporal and frontal cortex. The M cell pathways from V1 and the SC informed the dorsal stream of cortical processing involving MT, surrounding temporal cortex, and parietal–frontal sensorimotor domains. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Vision ◽  
2019 ◽  
Vol 4 (1) ◽  
pp. 3 ◽  
Author(s):  
Jon H. Kaas ◽  
Mary K. L. Baldwin

Current evidence supports the view that the visual pulvinar of primates consists of at least five nuclei, with two large nuclei, lateral pulvinar ventrolateral (PLvl) and central lateral nucleus of the inferior pulvinar (PIcl), contributing mainly to the ventral stream of cortical processing for perception, and three smaller nuclei, posterior nucleus of the inferior pulvinar (PIp), medial nucleus of the inferior pulvinar (PIm), and central medial nucleus of the inferior pulvinar (PIcm), projecting to dorsal stream visual areas for visually directed actions. In primates, both cortical streams are highly dependent on visual information distributed from primary visual cortex (V1). This area is so vital to vision that patients with V1 lesions are considered “cortically blind”. When the V1 inputs to dorsal stream area middle temporal visual area (MT) are absent, other dorsal stream areas receive visual information relayed from the superior colliculus via PIp and PIcm, thereby preserving some dorsal stream functions, a phenomenon called “blind sight”. Non-primate mammals do not have a dorsal stream area MT with V1 inputs, but superior colliculus inputs to temporal cortex can be more significant and more visual functions are preserved when V1 input is disrupted. The current review will discuss how the different visual streams, especially the dorsal stream, have changed during primate evolution and we propose which features are retained from the common ancestor of primates and their close relatives.


2021 ◽  
Author(s):  
Esmaeil Farhang ◽  
Ramin Toosi ◽  
Behnam Karami ◽  
Roxana Koushki ◽  
Ehsan Rezayat ◽  
...  

ABSTRACTTo expand our knowledge about the object recognition, it is critical to understand the role of spatial frequency (SF) in an object representation that occurs in the inferior temporal (IT) cortex at the final stage of processing the visual information across the ventral visual pathway. Object categories are being recognized hierarchically in at least three levels of abstraction: superordinate (e.g., animal), mid-level (e.g., human face), and subordinate (e.g., face identity). Psychophysical studies have shown rapid access to mid-level category information and low SF (LSF) contents. Although the hierarchical representation of categories has been shown to exist inside the IT cortex, the impact of SF on the multi-level category processing is poorly understood. To gain a deeper understanding of the neural basis of the interaction between SF and category representations at multiple levels, we examined the neural responses within the IT cortex of macaque monkeys viewing several SF-filtered objects. Each stimulus could be either intact or bandpass filtered into either the LSF (coarse shape information) or high SF (HSF) (fine shape information) bands. We found that in both High- and Low-SF contents, the advantage of mid-level representation has not been violated. This evidence suggests that mid-level category boundary maps are strongly represented in the IT cortex and remain unaffected with respect to any changes in the frequency content of stimuli. Our observations indicate the necessity of the HSF content for the superordinate category representation inside the IT cortex. In addition, our findings reveal that the representation of global category information is more dependent on the HSF than the LSF content. Furthermore, the lack of subordinate representation in both LSF and HSF filtered stimuli compared to the intact stimuli provide strong evidence that all SF contents are necessary for fine category visual processing.


2012 ◽  
Vol 279 (1737) ◽  
pp. 2289-2298 ◽  
Author(s):  
A. D. Milner

There are two highly interconnected clusters of visually responsive areas in the primate cortex. These two clusters have relatively few interconnections with each other, though those interconnections are undoubtedly important. One of the two main clusters (the dorsal stream) links the primary visual cortex (V1) to superior regions of the occipito-parietal cortex, while the other (the ventral stream) links V1 to inferior regions of the occipito-temporal cortex. According to our current understanding of the functional anatomy of these two systems, the dorsal stream's principal role is to provide real-time ‘bottom-up’ visual guidance of our movements online. In contrast, the ventral stream, in conjunction with top-down information from visual and semantic memory, provides perceptual representations that can serve recognition, visual thought, planning and memory offline. In recent years, this interpretation, initially based chiefly on studies of non-human primates and human neurological patients, has been well supported by functional MRI studies in humans. This perspective presents empirical evidence for the contention that the dorsal stream governs the visual control of movement without the intervention of visual awareness.


2018 ◽  
Author(s):  
Simona Monaco ◽  
Ying Chen ◽  
Nicholas Menghi ◽  
J Douglas Crawford

AbstractSensorimotor integration involves feedforward and reentrant processing of sensory input. Grasp-related motor activity precedes and is thought to influence visual object processing. Yet, while the importance of reentrant feedback is well established in perception, the top-down modulations for action and the neural circuits involved in this process have received less attention. Do action-specific intentions influence the processing of visual information in the human cortex? Using a cue-separation fMRI paradigm, we found that action-specific instruction (manual alignment vs. grasp) influences the cortical processing of object orientation several seconds after the object had been viewed. This influence occurred as early as in the primary visual cortex and extended to ventral and dorsal visual stream areas. Importantly, this modulation was unrelated to non-specific action planning. Further, the primary visual cortex showed stronger functional connectivity with frontal-parietal areas and the inferior temporal cortex during the delay following orientation processing for align than grasping movements, strengthening the idea of reentrant feedback from dorsal visual stream areas involved in action. To our knowledge, this is the first demonstration that intended manual actions have such an early, pervasive, and differential influence on the cortical processing of vision.


2019 ◽  
Author(s):  
Amarender R. Bogadhi ◽  
Leor N. Katz ◽  
Anil Bollimunta ◽  
David A. Leopold ◽  
Richard J. Krauzlis

AbstractThe evolution of the primate brain is marked by a dramatic increase in the number of neocortical areas that process visual information 1. This cortical expansion supports two hallmarks of high-level primate vision – the ability to selectively attend to particular visual features 2 and the ability to recognize a seemingly limitless number of complex visual objects 3. Given their prominent roles in high-level vision for primates, it is commonly assumed that these cortical processes supersede the earlier versions of these functions accomplished by the evolutionarily older brain structures that lie beneath the cortex. Contrary to this view, here we show that the superior colliculus (SC), a midbrain structure conserved across all vertebrates 4, is necessary for the normal expression of attention-related modulation and object selectivity in a newly identified region of macaque temporal cortex. Using a combination of psychophysics, causal perturbations and fMRI, we identified a localized region in the temporal cortex that is functionally dependent on the SC. Targeted electrophysiological recordings in this cortical region revealed neurons with strong attention-related modulation that was markedly reduced during attention deficits caused by SC inactivation. Many of these neurons also exhibited selectivity for particular visual objects, and this selectivity was also reduced during SC inactivation. Thus, the SC exerts a causal influence on high-level visual processing in cortex at a surprisingly late stage where attention and object selectivity converge, perhaps determined by the elemental forms of perceptual processing the SC has supported since before there was a neocortex.


2011 ◽  
Vol 23 (11) ◽  
pp. 3410-3418 ◽  
Author(s):  
Greg L. West ◽  
Adam A. K. Anderson ◽  
Susanne Ferber ◽  
Jay Pratt

When multiple stimuli are concurrently displayed in the visual field, they must compete for neural representation at the processing expense of their contemporaries. This biased competition is thought to begin as early as primary visual cortex, and can be driven by salient low-level stimulus features. Stimuli important for an organism's survival, such as facial expressions signaling environmental threat, might be similarly prioritized at this early stage of visual processing. In the present study, we used ERP recordings from striate cortex to examine whether fear expressions can bias the competition for neural representation at the earliest stage of retinotopic visuo-cortical processing when in direct competition with concurrently presented visual information of neutral valence. We found that within 50 msec after stimulus onset, information processing in primary visual cortex is biased in favor of perceptual representations of fear at the expense of competing visual information (Experiment 1). Additional experiments confirmed that the facial display's emotional content rather than low-level features is responsible for this prioritization in V1 (Experiment 2), and that this competition is reliant on a face's upright canonical orientation (Experiment 3). These results suggest that complex stimuli important for an organism's survival can indeed be prioritized at the earliest stage of cortical processing at the expense of competing information, with competition possibly beginning before encoding in V1.


2021 ◽  
Vol 1 (1) ◽  
Author(s):  
Melvyn A. Goodale

AbstractThe visual guidance of goal-directed movements requires transformations of incoming visual information that are different from those required for visual perception. For us to grasp an object successfully, our brain must use just-in-time computations of the object’s real-world size and shape, and its orientation and disposition with respect to our hand. These requirements have led to the emergence of dedicated visuomotor modules in the posterior parietal cortex of the human brain (the dorsal visual stream) that are functionally distinct from networks in the occipito-temporal cortex (the ventral visual stream) that mediate our conscious perception of the world. Although the identification and selection of goal objects and an appropriate course of action depends on the perceptual machinery of the ventral stream and associated cognitive modules, the execution of the subsequent goal-directed action is mediated by dedicated online control systems in the dorsal stream and associated motor areas. The dorsal stream allows an observer to reach out and grasp objects with exquisite ease, but by itself, deals only with objects that are visible at the moment the action is being programmed. The ventral stream, however, allows an observer to escape the present and bring to bear information from the past – including information about the function of objects, their intrinsic properties, and their location with reference to other objects in the world. Ultimately then, both streams contribute to the production of goal-directed actions. The principles underlying this division of labour between the dorsal and ventral streams are relevant to the design and implementation of autonomous robotic systems.


2007 ◽  
Vol 98 (3) ◽  
pp. 1253-1262 ◽  
Author(s):  
Robin Laycock ◽  
David P. Crewther ◽  
Paul B. Fitzgerald ◽  
Sheila G. Crewther

Evidence from human and primate studies suggests that fast visual processing may utilize signals projecting from primary visual cortex (V1) through the dorsal stream, to area V5/MT+ or beyond and subsequently back into V1. This coincides with the arrival of parvocellular signals en route to the ventral pathway and infero-temporal cortex. Such evidence suggests that the dorsal stream region V5/MT+ is activated rapidly through the traditional hierarchical pathway and also via a less-well-established direct signal to V5/MT+ bypassing V1. To test this, 16 healthy humans underwent transcranial magnetic stimulation (TMS) of V1/V2 and V5/MT+ while performing a motion-direction detection task. A three-alternate forced-choice design (left/right motion, stationary) allowed analysis of the quality of errors made, in addition to the more usual performance measures. Transient disruption of V1/V2 and V5/MT+ significantly reduced accuracy when TMS was applied at or near motion onset. Most participants also showed disrupted performance with TMS application over V1/V2 ∼125 ms post motion onset, and significantly reduced accuracy at 158 ms with V5/MT+ stimulation. The two periods of disruption with V1/V2 TMS are suggestive of feedforward/feedback models, although the earlier period of disruption has not been reported in previous TMS studies. Very early activation of V5/MT+, evidenced by diminished accuracy and reduced perception of motion after TMS may be indicative of a thalamic-extrastriate pathway in addition to the traditionally expected later period of processing. A profound disruption of performance prestimulus onset is more likely to reflect disruption of top-down expectancy than disruption of visual processing.


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