Silvia Savazzi

Collicular vision guides nonconscious behavior

Following destruction or deafferentation of primary visual cortex (area V1, striate cortex), clinical blindness ensues, but residual visual functions may, nevertheless, persist without perceptual consciousness (a condition termed blindsight). The study of patients with such lesions thus offers a unique opportunity to investigate what visual capacities are mediated by the extrastriate pathways that bypass V1. Here we provide evidence for a crucial role of the collicular–extrastriate pathway in nonconscious visuomotor integration by showing that, in the absence of V1, the superior colliculus (SC) is essential to translate visual signals that cannot be consciously perceived into motor outputs. We found that a gray stimulus presented in the blind field of a patient with unilateral V1 loss, although not consciously seen, can influence his behavioral and pupillary responses to consciously perceived stimuli in the intact field (implicit bilateral summation). Notably, this effect was accompanied by selective activations in the SC and in occipito-temporal extrastriate areas. However, when instead of gray stimuli we presented purple stimuli, which predominantly draw on S-cones and are thus invisible to the SC, any evidence of implicit visuomotor integration disappeared and activations in the SC dropped significantly. The present findings show that the SC acts as an interface between sensory and motor processing in the human brain, thereby providing a contribution to visually guided behavior that may remain functionally and anatomically segregated from the geniculo-striate pathway and entirely outside conscious visual experience.

Attention and Interhemispheric Transfer: A Behavioral and fMRI Study

When both detections and responses to visual stimuli are performed within one and the same hemisphere, manual reaction times (RTs) are faster than when the two operations are carried out in different hemispheres. A widely accepted explanation for this difference is that it reflects the time lost in callosal transmission. Interhemispheric transfer time can be estimated by subtracting RTs for uncrossed from RTs for crossed responses (crossed uncrossed difference, or CUD). In the present study, we wanted to ascertain the role of spatial attention in affecting the CUD and to chart the brain areas whose activity is related to these attentional effects on interhemispheric transfer. To accomplish this, we varied the proportion of crossed and uncrossed trials in different blocks. With this paradigm subjects are likely to focus attention either on the hemifield contralateral to the responding hand (blocks with 80 crossed trials) or on the ipsilateral hemifield (blocks with 80 uncrossed trials). We found an inverse correlation between the proportion of crossed trials in a block and the CUD and this effect can be attributed to spatial attention. As to the imaging results, we found that in the crossed minus uncrossed subtraction, an operation that highlights the neural processes underlying interhemispheric transfer, there was an activation of the genu of the corpus callosum as well as of a series of cortical areas. In a further commonality analysis, we assessed those areas which were activated specifically during focusing of attention onto one hemifield either contra- or ipsilateral to the responding hand. We found an activation of a number of cortical and subcortical areas, notably, parietal area BA 7 and the superior colliculi. We believe that the main thrust of the present study is to have teased apart areas important in interhemispheric transmission from those involved in spatial attention.

The superior colliculus subserves interhemispheric neural summation in both normals and patients with a total section or agenesis of the corpus callosum.

To verify the possibility that the superior colliculus (SC) subserves interhemispheric neural summation, we presented single or double white visual targets to one or both hemifields in normal participants and in patients lacking the corpus callosum (one with total callosotomy and one with callosal agenesis). Simple reaction time was typically faster with double than single stimuli, a phenomenon known as the redundant target effect (RTE); moreover, confirming previous results, we found a larger RTE in patients without callosum than in normals. In both groups, the redundancy gain was related to neural coactivation rather than to probability summation. The novel finding was that, when using monochromatic purple stimuli that are invisible to the SC, we found a similar redundancy gain in both groups; moreover, this redundancy gain was probabilistic rather than neural. Control experiments with monochromatic red stimuli yielded a RTE of the neural type similar to that with white stimuli and this confirmed that the probabilistic RTE found was specific for purple stimuli. In conclusion, visual input to the SC is necessary for interhemispheric neural summation in both normals and in individuals without the corpus callosum while probabilistic summation can occur without a collicular contribution.

Speeding up reaction time with invisible stimuli

Normal subjects react more quickly to a pair of visual stimuli than to a stimulus alone. This phenomenon is known as the redundant signal effect (RSE) and represents an example of divided visual attention in which signal processing is carried out in parallel to the advantage of response speed. A most interesting aspect of this phenomenon is that it can occur when one stimulus in a pair cannot be consciously detected because of hemianopia or unilateral extinction resulting from brain damage. Here, we report that a similar dissociation between visual awareness and visually guided behavior is present in normal subjects who show an RSE even when the luminance of one of a pair of stimuli is below detection threshold. The observed RSE cannot be attributed to probability summation because it violates Millers race inequality and is likely to be related to neural summation between supra- and subthreshold stimuli. Given that a similar implicit RSE is present in hemispherectomy patients, we hypothesize that the site of this summation might be the superior colliculus (SC).

Interhemispheric transfer following callosotomy in humans: Role of the superior colliculus

It is now common knowledge that the total surgical section of the corpus callosum (CC) and of the other forebrain commissures prevents interhemispheric transfer (IT) of a host of mental functions. By contrast, IT of simple sensorimotor functions, although severely delayed, is not abolished, and an important question concerns the pathways subserving this residual IT. To answer this question we assessed visuomotor IT in split-brain patients using the Poffenberger paradigm (PP), that is, a behavioral paradigm in which simple reaction time (RT) to visual stimuli presented to the hemifield ipsilateral to the responding hand is compared to stimuli presented to the contralateral hemifield, a condition requiring an IT. We tested the possibility that the residual IT is mediated by the collicular commissure interconnecting the two sides of the superior colliculus (SC). To this purpose, we used short-wavelength visual stimuli, which in neurophysiological studies in non-human primates have been shown to be undetectable by collicular neurons. We found that, in both totally and partially callosotomised patients, IT was considerably longer with S-cone input than with L-cone input or with achromatic stimuli. This was not the case in healthy participants in whom IT was not affected by color. These data clearly show that the SC plays an important role in IT of sensorimotor information in the absence of the corpus callosum.

The sleep-deprived brain in normals and patients with juvenile myoclonic epilepsy: A perturbational approach to measuring cortical reactivity

Simultaneous electroencephalography-transcranial magnetic stimulation (EEG-TMS) investigates cortical reactivity to external perturbations. TMS evoked potentials (TEPs) have been described in normals during sleep and wake but not after sleep deprivation or in pathologically enhanced excitability, i.e., epilepsy. The aim of our study was to identify TEPs and their modifications via EEG-TMS co-registration in healthy controls and patients with juvenile myoclonic epilepsy (JME) during wake, sleep deprivation and sleep conditions. Focal TMS was administered to the primary motor cortex in 12 healthy controls and 10 patients with JME. At least 150 TMS were delivered randomly every 8-15s during wake, sleep deprivation and sleep conditions. EEG was simultaneously acquired from 32 scalp electrodes. A significant increase in late peak amplitudes (P100 and N190) was observed in all subjects during the sleep-deprived condition, with a marked anterior increase and overall higher amplitude potentials in the JME patients. We demonstrated an overall higher cortical excitability in the JME patients, particularly over the anterior cortex after sleep deprivation and rebound sleep. This phenomenon could be related to the cortico-thalamic circuit dysfunctions believed to cause myoclonic epilepsy and a higher susceptibility of the frontal and prefrontal areas to the effects of sleep deprivation.

Is audiovisual integration subserved by the superior colliculus in humans

The brain effectively integrates multisensory information to enhance perception. For example, audiovisual stimuli typically yield faster responses than isolated unimodal ones (redundant signal effect, RSE). Here, we show that the audiovisual RSE is likely subserved by a neural site of integration (neural coactivation), rather than by an independent-channels mechanism such as race models. This neural site is probably the superior colliculus (SC), because an RSE explainable by neural coactivation does not occur with purple or blue stimuli, which are invisible to the SC; such an RSE only occurs for spatially and temporally coincident audiovisual stimuli, in strict adherence with the multisensory responses in the SC of the cat. These data suggest that audiovisual integration in humans occurs very early during sensory processing, in the SC.

Reaction time inhibition from subliminal cues: Is it related to inhibition of return?

Task-irrelevant visual cues with near zero visibility proved apt to retard reaction time for the detection of supraliminal visual targets presented at the cued location. The time course of the effect was similar to that of the so-called inhibition-of return (IOR), which is assumed to be due to the withdrawal of attention from the inhibited location. However the present subliminal cues consistently failed to induce an RT facilitation prior to the RT inhibition, contrary to what would be expected if the cue were able to attract attention to the cued location. Since the RT inhibition from subliminal cues could not be attributed to the withdrawal of attention from the cued location, it can be argued that such cues acted both outside of consciousness and without the influence of attention. Therefore, the RT inhibitory effect seems best accounted for by an automatic, unconscious and attention-independent self-inhibition of response tendencies instructed by irrelevant information, akin to that postulated by (Eimer, M., & Schlaghecken, F. (1998). Effects of masked stimuli on motor activation: behavioural and electrophysiological evidence. Journal of Experimental Psychology Human Perception and Performance, 24, 1737-1747.) to explain the negative compatibility effect.

The role of the magnocellular and parvocellular systems in the redundant target effect

The redundant target effect (RTE) consists in the speeding of reaction time with single versus multiple targets and can be explained either by a neural coactivation or by a race model. To try to understand the role of the magnocellular and parvocellular systems in the determination of the RTE we carried out three experiments using onset or feature singletons. The former are likely to be mainly processed by the magnocellular system while the latter are mainly processed by the parvocellular system. In experiment 1 we found an RTE both when the target (red disk) was presented in isolation and when it was surrounded by equiluminant green distractors. Thus, the RTE occurred both with onset and feature singletons. However, with the former, the RTE could be accounted for by neural coactivation while with the latter it could be accounted for by a probabilistic explanation. In experiment 2 we tried to ascertain the role of distractors in yielding a probabilistic RTE: we used either targets in isolation or surrounded by distractors of lower luminance and found an RTE that could be explained by neural coactivation for both kinds of targets. This ruled out an effect of distractors per se in determining a probabilistic RTE. Finally, in experiment 3 we used targets of lower luminance than either the background or the distractors. We found that the RTE could be accounted for by neural coactivation with targets alone while it was probabilistic with distractors. Overall, these results show that stimuli presumably processed by the magnocellular system yield redundancy gains that result from a neural coactivation mechanism. In contrast, stimuli presumably processed by the parvocellular system are compatible with a probabilistic redundancy gain.

TMS modulation of visual and auditory processing in the posterior parietal cortex

Audio-visual stimuli typically yield faster responses than isolated modality-specific ones. This crossmodal speed advantage depends upon efficient multisensory integration mechanisms in the brain. Here, we used repetitive transcranial magnetic stimulation (rTMS) to address the role of the posterior parietal cortex, in particular of the inferior parietal lobule (IPL), in speeding up responses to crossmodal stimuli. The results show that rTMS over IPL impairs the response to contralateral modality-specific visual and auditory targets without affecting the response speed advantage following audio-visual targets. Furthermore, this speed advantage is subserved by a neural coactivation mechanism suggesting a summation in a given neural site. Control rTMS over V1 impaired only contralateral visual responses without affecting the response to auditory or audio-visual targets. These results suggest that the response speed advantage for crossmodal targets is maintained in spite of the IPL interference that impairs modality-specific responses. The possible role of alternative sites for the audio-visual advantage, such as the superior colliculus, is discussed.