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

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’.

The Evolution of the Pulvinar Complex in Primates and Its Role in the Dorsal and Ventral Streams of Cortical Processing

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.

Attention enhances LFP phase coherence in macaque visual cortex, improving sensory processing

Attention selectively routes the most behaviorally relevant information among the vast pool of sensory inputs through cortical regions. Previous studies have shown that visual attention samples the surrounding stimuli periodically. However, the neural mechanism underlying this sampling in the sensory cortex, and whether the brain actively uses these rhythms, has remained elusive. Here, we hypothesize that selective attention controls the phase of oscillatory synaptic activities to efficiently process the relevant information in the brain. We document an attentional modulation of pre-stimulus inter-trial phase coherence (a measure of deviation between instantaneous phases of trials) at low frequencies in macaque visual area MT. Our data reveal that phase coherence increases when attention is deployed towards the receptive field of the recorded neural population. We further show that the attentional enhancement of phase coherence is positively correlated with the attentional modulation of stimulus induced firing rate, and importantly, a higher phase coherence leads to a faster behavioral response. Our results suggest a functional utilization of intrinsic neural oscillatory activities for better processing upcoming environmental stimuli, generating the optimal behavior.

A circuit for saccadic suppression in the primate brain

Saccades should cause us to see a blur as the eyes sweep across a visual scene. Specific brain mechanisms prevent this by producing suppression during saccades. Neuronal correlates of such suppression were first established in the visual superficial layers of the superior colliculus (SC) and subsequently have been observed in cortical visual areas, including the middle temporal visual area (MT). In this study, we investigated suppression in a recently identified circuit linking visual SC (SCs) to MT through the inferior pulvinar (PI). We examined responses to visual stimuli presented just before saccades to reveal a neuronal correlate of suppression driven by a copy of the saccade command, referred to as a corollary discharge. We found that visual responses were similarly suppressed in SCs, PI, and MT. Within each region, suppression of visual responses occurred with saccades into both visual hemifields, but only in the contralateral hemifield did this suppression consistently begin before the saccade (~100 ms). The consistency of the signal along the circuit led us to hypothesize that the suppression in MT was influenced by input from the SC. We tested this hypothesis in one monkey by inactivating neurons within the SC and found evidence that suppression in MT depends on corollary discharge signals from motor SC (SCi). Combining these results with recent findings in rodents, we propose a complete circuit originating with corollary discharge signals in SCi that produces suppression in visual SCs, PI, and ultimately, MT cortex. NEW & NOTEWORTHY A fundamental puzzle in visual neuroscience is that we frequently make rapid eye movements (saccades) but seldom perceive the visual blur accompanying each movement. We investigated neuronal correlates of this saccadic suppression by recording from and perturbing a recently identified circuit from brainstem to cortex. We found suppression at each stage, with evidence that it was driven by an internally generated signal. We conclude that this circuit contributes to neuronal suppression of visual signals during eye movements.

Visual impairment by surrounding noise is due to interactions among stimuli in the higher-order visual cortex

Observers have difficulty identifying a target in their peripheral vision in the presence of surrounding stimuli. Although hypotheses addressing this phenomenon have been proposed, such as the integration of stimuli and surround suppression in the higher-order visual cortex, no direct comparisons of the psychophysical and neuronal sensitivities have been performed. Here we measured the performance of monkeys with a variant of the direction discrimination task using a center/surround bipartite random-dot stimulus while simultaneously recording from isolated neurons from the middle temporal visual area (MT). The psychophysical threshold increased with the addition of a task-irrelevant noise annulus that surrounded the task-relevant motion stimuli. The neuronal threshold of MT neurons also increased at a spatial scale similar to the psychophysical threshold. This suggests that the impaired ability in our task resulted from impairment in the MT area. Importantly, reduced neuronal performance was due to both a reduced response to preferred motion and an enhanced response to nonpreferred motion. These observations suggest that impairment caused by surrounding noise results from interactions between stimuli and noise and not from a reduction in the response of visual neurons.