Seeing without a Scene: Neurological Observations on the Origin and Function of the Dorsal Visual Stream.

In all vertebrates, visual signals from each visual field project to the opposite midbrain tectum (called the superior colliculus in mammals). The tectum/colliculus computes visual salience to select targets for context-contingent visually guided behavior: a frog will orient toward a small, moving stimulus (insect prey) but away from a large, looming stimulus (a predator). In mammals, visual signals competing for behavioral salience are also transmitted to the visual cortex, where they are integrated with collicular signals and then projected via the dorsal visual stream to the parietal and frontal cortices. To control visually guided behavior, visual signals must be encoded in body-centered (egocentric) coordinates, and so visual signals must be integrated with information encoding eye position in the orbit-where the individual is looking. Eye position information is derived from copies of eye movement signals transmitted from the colliculus to the frontal and parietal cortices. In the intraparietal cortex of the dorsal stream, eye movement signals from the colliculus are used to predict the sensory consequences of action. These eye position signals are integrated with retinotopic visual signals to generate scaffolding for a visual scene that contains goal-relevant objects that are seen to have spatial relationships with each other and with the observer. Patients with degeneration of the superior colliculus, although they can see, behave as though they are blind. Bilateral damage to the intraparietal cortex of the dorsal stream causes the visual scene to disappear, leaving awareness of only one object that is lost in space. This tutorial considers what we have learned from patients with damage to the colliculus, or to the intraparietal cortex, about how the phylogenetically older midbrain and the newer mammalian dorsal cortical visual stream jointly coordinate the experience of a spatially and temporally coherent visual scene.

Indignation for moral violations suppresses the tongue motor cortex: preliminary TMS evidence.

We commonly label moral violations in terms of 'disgust', yet it remains unclear whether metaphorical expressions linking disgust and morality are genuinely shared at the cognitive/neural level. Using transcranial magnetic stimulation (TMS), we provide new insights into this debate by measuring motor-evoked potentials (MEPs) from the tongue generated by TMS over the tongue primary motor area (tM1) in a small group of healthy participants presented with vignettes of moral transgressions and non-moral vignettes. We tested whether moral indignation, felt while evaluating moral vignettes, affected tM1 excitability. Vignettes exerted a variable influence on MEPs with no net effect of the moral category. However, in accordance with our recent study documenting reduced tM1 excitability during exposure to pictures of disgusting foods or facial expressions of distaste, we found that the vignettes of highly disapproved moral violations reduced tM1 excitability. Moreover, tM1 excitability and moral indignation were linearly correlated: the higher the moral indignation, the lower the tM1 excitability. Respective changes in MEPs were not observed in a non-oral control muscle, suggesting a selective decrease of tM1 excitability. These preliminary findings provide neurophysiological evidence supporting the hypothesis that morality might have originated from the more primitive experience of oral distaste.

Patients with lesions to the intraparietal cortex show greater proprioceptive realignment after prism adaptation: Evidence from open-loop pointing and manual straight ahead.

Reaching toward a target viewed through laterally refracting prisms results in adaptation of both visual and (limb) proprioceptive spatial representations. Common ways to measure adaptation after-effect are to ask a person to point straight ahead with their eyes closed ("manual straight ahead", MSA), or to a seen target using their unseen hand ("open-loop pointing", OLP). MSA measures changes in proprioception only, whereas OLP measures the combined visual and proprioceptive shift. The behavioural and neurological mechanisms of prism adaptation have come under scrutiny following reports of reduced hemispatial neglect in patients following this procedure. We present evidence suggesting that shifts in proprioceptive spatial representations induced by prism adaptation are larger following lesions to the intraparietal cortex - a brain region that integrates retinotopic visual signals with signals of eye position in the orbit and that is activated during prism adaptation. Six healthy participants and six patients with unilateral intraparietal cortex lesions underwent prism adaptation. After-effects were measured with OLP and MSA. After-effects of control participants were larger when measured with OLP than with MSA, consistent with previous research and with the additional contribution of visual shift to OLP after-effects. However, patients' OLP shifts were not significantly different to their MSA shifts. We conclude that, for the patients, correction of pointing errors during prism adaptation involved proportionally more changes to arm proprioception than for controls. Since lesions to intraparietal cortex led to enhanced realignment of arm proprioceptive representations, our results indirectly suggest that the intraparietal cortex could be key for visual realignment.

Intact tactile detection yet biased tactile localization in a hand-centered frame of reference: Evidence from a dissociation.

We examined the performance of an individual with subcortical damage, but an intact somatosensory thalamocortical pathway, to examine the functional architecture of tactile detection and tactile localization processes. Consistent with the intact somatosensory thalamocortical pathway, tactile detection on the contralesional hand was well within the normal range. Despite intact detection, the individual demonstrated substantial localization biases. Across all localization experiments, he consistently localized tactile stimuli to the left side in space relative to the long axis of his hand. This was observed when the contralesional hand was palm up, palm down, rotated 90° relative to the trunk, and when making verbal responses. Furthermore, control experiments demonstrated that this response pattern was unlikely a motor response error. These findings indicate that tactile localization on the body is influenced by proprioceptive information specifically in a hand-centered frame of reference. Furthermore, this also provides evidence that aspects of tactile localization are mediated by pathways outside of the primary somatosensory thalamocortical pathway.

Circadian circuits in humans: White matter microstructure predicts daytime sleepiness.

The suprachiasmatic nucleus of the hypothalamus is the chief circadian pacemaker in the brain, and is entrained to day-night cycles by visual afferents from melanopsin containing retinal ganglion cells via the inferior accessory optic tract. Tracer studies have demonstrated efferents from the suprachiasmatic nucleus projecting to the paraventricular nucleus of the hypothalamus, which in turn project to first-order sympathetic neurons in the intermedio-lateral grey of the spinal cord. Sympathetic projections to the pineal gland trigger the secretion of the sleep inducing hormone melatonin. The current study reports the first demonstration of potential sympathopetal hypothalamic projections involved in circadian regulation in humans with in vivo virtual white matter dissections using probabilistic diffusion tensor imaging (DTI) tractography. Additionally, our data shows a correlation between individual differences in white matter microstructure (measured with fractional anisotropy) and increased daytime sleepiness [measured with the Epworth Sleepiness Scale (ESS, Johns, 1991)]. Sympathopetal connections with the hypothalamus were virtually dissected using designated masks on the optic chiasm, which served as an anatomical landmark for retinal fibres projecting to the suprachiasmatic nucleus, and a waypoint mask on the lateral medulla, where hypothalamic projections to the sympathetic nervous system traverse in humans. Sympathopetal projections were demonstrated in each hemisphere in twenty-six subjects. The tract passed through the suprachiasmatic nucleus of the hypothalamus and its trajectory corresponds to the dorsal longitudinal fasciculus traversing the periaqueductal region and the lateral medulla. White matter microstructure (FA) in the left hemisphere correlated with high scores on the ESS, suggesting an association between circadian pathway white matter microstructure, and increased daytime sleepiness.

Stria terminalis microstructure in humans predicts variability in orienting towards threat.

Current concepts of the extended amygdala posit that basolateral to central amygdala projections mediate fear-conditioned autonomic alerting, whereas projections to the bed nucleus of the stria terminalis mediate sustained anxiety. Using diffusion tensor imaging tractography in humans, we show that microstructure of the stria terminalis correlates with an orienting bias towards threat in a saccade decision task, providing the first evidence that this circuit supports decisions guiding evaluation of threatening stimuli.

The effect of prism adaptation on state estimates of eye position in the orbit.

Prism adaptation (PA) after-effects are assessed using tests that measure changes in sensorimotor systems. After-effects on pointing without feedback to a visual target (open loop pointing - OLP) are traditionally described as being larger than those measured by straight ahead pointing (SAP) with eyes closed, and the difference between them is attributed to a shift in visual localisation. However, neither differences between OLP and SAP, nor shifts in perceptual judgement of visual straight ahead (VSA), are consistently reported. Moreover, since very few studies have directly recorded direction of gaze, an effect of PA on the state estimate of gaze direction has not been reliably documented. The current research aimed to isolate the effects of PA on state estimates of eye position. We measured sensorimotor after-effects through common (OLP, SAP, and VSA) measures, and also recorded eye position and additional after-effect measures to interrogate changes to the oculomotor system and how these might relate to other measures of sensorimotor change. To ascertain if PA's effects on estimates of eye position could be attributed to eye muscle potentiation, we compared the effects of PA to sustained gaze deviation without adaptation. PA induced no effect on visual straight-ahead and no change in direction of gaze, when measured while positioning a target, looking straight ahead in the dark, or looking toward the passively positioned and occluded unexposed hand. We also found that after-effects measured by SAP with the eyes open were larger than SAP with the eyes closed and equal to those observed with OLP. The findings challenge the concept that total adaptation after-effect is a direct sum of arm proprioceptive and visual after-effects as conventionally measured, and suggest that the oculomotor system is altered by prism adaptation only in interaction with an arm motor command when vision is available.

Orienting toward threat: Contributions of a subcortical pathway transmitting retinal afferents to the amygdala via the superior colliculus and pulvinar.

Probabilistic diffusion tractography was used to provide the first direct evidence for a subcortical pathway from the retina to the amygdala, via the superior colliculus and pulvinar, that transmits visual stimuli signaling threat. A bias to orient toward threat was measured in a temporal order judgement saccade decision task, under monocular viewing, in a group of 19 healthy participants who also underwent diffusion weighted MR imaging. On each trial of the behavioural task a picture depicting threat was presented in one visual field and a competing non-threatening stimulus in the other. The onset interval between the two pictures was randomly varied and participants made a saccade toward the stimulus that they judged to have appeared first. The bias to orient toward threat was stronger when the threatening stimulus was in the temporal visual hemifield, suggesting that afferents via the retinotectal tract contributed to the bias. Probabalistic tractography was used to virtually dissect connections between the superior colliculus and the amygdala traversing the pulvinar. Individual differences in microstructure (fractional anisotropy) of the streamline predicted the magnitude of the bias to orient toward threat, providing supporting evidence for a functional role of the subcortical SC-amygdala pathway in processing threat in healthy humans.

Preserved re-experience of discrete emotions: Amnesia and executive function.

Amnesic patients can re-experience emotions elicited by forgotten events, suggesting that brain systems for episodic and emotional memory are independent. However, the range of such emotional memories remains under-investigated (most studies employing just positive-negative emotion dyads), and executive function may also play a role in the re-experience of emotions. This is the first investigation of the intensity of the emotional re-experience of a range of discrete emotions (anger, fear, sadness, and happiness) for a group of amnesic patients. Twenty Korsakoff syndrome (KS) patients and 20 neurologically normal controls listened to four novel emotional vignettes selectively eliciting the four basic emotions. Emotional experience was measured using pen-and-paper Visual Analogue Mood Scales and episodic memory using verbal recollections. After 30 min, the recollection of stories was severely impaired for the patient group, but the emotional re-experience was no different from that of controls. Notably, there was no relationship between episodic recall and the intensity of the four emotions, such that even profoundly amnesic patients reported moderate levels of the target emotion. Exploratory analyses revealed negative correlations between the intensity of basic emotions and executive functions (e.g., cognitive flexibility and response inhibition) for controls but not patients. The results suggest that discrete emotions can be re-experienced independently of episodic memory, and that the re-experience of certain discrete emotions appears to be dampened by executive control. KS patients with absent or mild cognitive symptoms should benefit from emotion-regulation interventions aimed at reducing the recognized affective burden associated with their episodic memory deficit.

Saccade latency bias toward temporal hemifield: Evidence for role of retinotectal tract in mediating reflexive saccades.

The superior colliculus (SC) plays a critical role in mediating reflexive eye movements. Under optimal conditions, for example including a temporal 'gap' of 200 ms after fixation offset and prior to target onset, it is possible to isolate a population of 'express saccades' with very short latencies between 80 and 120 ms. Ablation of the SC abolishes express saccades in monkeys. However, it remains to be established whether express saccade generation is dependent upon visual afferents transmitting direct retinal projections to SC via the retinotectal tract (RTT). In nineteen healthy human participants, we used a gap paradigm to investigate whether express saccades demonstrate shorter latencies to targets in the temporal hemifield, a marker for RTT function. A population of predominantly reflexive saccades (with latencies between 70 and 150 ms) was isolated in which latencies toward temporal hemifield targets were shown to be shorter than toward nasal hemifield targets. The advantages for reflexive saccades toward temporal hemifield targets suggest that visual efferents from the retina to the superior colliculus contribute to generating reflexively triggered saccades.

An Opponent Process Cerebellar Asymmetry for Regulating Word Association Priming.

A consensus has emerged that the cerebellum makes important contributions to a spectrum of linguistic processes, but that the psychobiology of these contributions remains enigmatic (Mariën et al., Cerebellum 13(3):386-410, 2014). One aspect of this enigma arises from the fact that, although the language-dominant left cerebral hemisphere is connected to the right cerebellum, distinctive contributions of the left cerebellar hemisphere have been documented (Murdoch and Whelan, Folia Phoniatr Logop 59:184-9, 2007), but remain poorly understood. Here, we report that neurodisruption of the left and right cerebellar hemispheres have opposite effects on associative word priming in a lexical decision task. Reaction time was measured for decisions on whether a target letter string constituted a word (e.g. bread) or, with equal probability, a pronounceable non-word (e.g. dreab). A prime word was presented for 150 ms before the target and could either, and with equal probability, be related (e.g. BUTTER) or unrelated (TRACTOR). Associative word priming was computed as the reduction in lexical decision RT on trials with related primes. Left cerebellar hemisphere continuous theta-burst transcranial magnetic stimulation (TMS) decreased, and right hemisphere stimulation increased, priming. The results suggest that the cerebellum contributes to predictive sequential processing, in this case language, through an opponent process mechanism coordinated by both cerebellar hemispheres.

Neuromodulation of Right Auditory Cortex Selectively Increases Activation in Speech-Related Brain Areas in Brainstem Auditory Agnosia.

Auditory agnosia is an inability to make sense of sound that cannot be explained by deficits in low-level hearing. In view of recent promising results in the area of neurorehabilitation of language disorders after stroke, we examined the effect of transcranial direct current stimulation (tDCS) in a young woman with general auditory agnosia caused by traumatic injury to the left inferior colliculus. Specifically, we studied activations to sound embedded in a block design using functional magnetic resonance imaging before and after application of anodal tDCS to the right auditory cortex. Before tDCS, auditory discrimination deficits were associated with abnormally reduced activations of the auditory cortex and bilateral unresponsiveness of the anterior superior temporal sulci and gyri. This session replicated a previous functional scan with the same paradigm a year before the current experiment. We then applied anodal tDCS over right auditory cortex for 20 min-utes and immediately re-scanned the patient. We found increased activation of bilateral auditory cortices and, for speech sounds, selectively increased activation in Broca's and Wernicke's areas. Future research might consider the long-term behavioral effects after neurostimulation in auditory agnosia and its potential use in the neurorehabilitation of more general auditory disorders.

The effect of hunger and satiety in the judgment of ethical violations.

Human history is studded with instances where instinctive motivations take precedence over ethical choices. Nevertheless, the evidence of any linking between motivational states and morality has never been systematically explored. Here we addressed this topic by testing a possible linking between appetite and moral judgment. We compared moral disapproval ratings (MDR) for stories of ethical violations in participants under fasting and after having eaten a snack. Our results show that subjective hunger, measured via self-reported rating, reduces MDR for ethical violations. Moreover, the higher the disgust sensitivity the higher the MDR for ethical violations. This study adds new insights to research on physiological processes influencing morality by showing that appetite affects moral disapproval of ethical violations.

Core, social and moral disgust are bounded: A review on behavioral and neural bases of repugnance in clinical disorders.

Disgust is a multifaceted experience that might affect several aspects of life. Here, we reviewed research on neurological and psychiatric disorders that are characterized by abnormal disgust processing to test the hypothesis of a shared neurocognitive architecture in the representation of three disgust domains: i) personal experience of 'core disgust'; ii) social disgust, i.e., sensitivity to others' expressions of disgust; iii) moral disgust, i.e., sensitivity to ethical violations. Our review provides some support to the shared neurocognitive hypothesis and suggests that the insula might be the "hub" structure linking the three domains of disgust sensitivity, while other brain regions may subserve specific facets of the multidimensional experience. Our review also suggests a role of serotonin core and moral disgust, supporting "neo-sentimentalist" theories of morality, which posit a causal role of affect in moral judgment.

Salivary secretion and disgust: A pilot study.

Although a direct link has been established between self-experienced disgust and salivary secretion, it is unclear whether this physiological index is modulated by the social experience of disgust (i.e., exposure to the facial expression of disgust). We tested this issue in a pilot study by collecting salivary samples in a group of 20 healthy humans watching pictures of faces expressing disgust. Moreover, we tried to replicate previous evidence by testing saliva secretion in response to pictures of unpalatable (i.e., rotten) food and non-gustatory disgusting stimuli (i.e., disgusting insects). Overall, our analysis shows a general reduction of saliva secretion in response to disgust stimuli, compared to their positive counterparts, although further analyses for specific stimulus categories indicated that this difference was statistically significant only for food pictures. The non-significance of the face and insect categories might be due to insufficient power of our small sample. Overall, a general reduction of saliva secretion for different disgust-related stimuli suggests a shared mechanism of encoding, in line with theories of neural reuse.

Deafferentation of the Superior Colliculus Abolishes Spatial Summation of Redundant Visual Signals.

Two visual signals appearing simultaneously are detected more rapidly than either signal appearing alone. Part of this redundant target effect (RTE) can be attributed to neural summation that has been proposed to occur in the superior colliculus (SC). We report direct evidence in two neurological patients for neural summation in the SC, and that it is mediated by afferent visual information transmitted through its brachium. The RTE was abolished in one patient with a hemorrhage involving the right posterior thalamus that damaged part of the SC and that disrupted its brachium; and in another patient in whom the SC appeared intact but deafferented due to traumatic avulsion of its brachium. In addition reaction time for unilateral targets in the contralesional field was slowed in both patients, providing the first evidence that visual afferents to the SC contribute to the efficiency of target detection.

Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex.

The tongue holds a unique role in gustatory disgust. However, it is unclear whether the tongue representation in the motor cortex (tM1) is affected by the sight of distaste-related stimuli. Using transcranial magnetic stimulation (TMS) in healthy humans, we recorded tongue motor-evoked potentials (MEPs) as an index of tM1 cortico-hypoglossal excitability. MEPs were recorded while participants viewed pictures associated with gustatory disgust and revulsion (i.e. rotten foods and faces expressing distaste), non-oral-related disgusting stimuli (i.e. invertebrates like worms) and control stimuli. We found that oral-related disgust pictures suppressed tM1 cortico-hypoglossal output. This tM1 suppression was predicted by interindividual differences in disgust sensitivity. No similar suppression was found for disgusting invertebrates or when MEPs were recorded from a control muscle. These findings suggest that revulsion-eliciting food pictures trigger anticipatory inhibition mechanisms, possibly preventing toxin swallowing and contamination. A similar suppression is elicited when viewing distaste expressions, suggesting vicarious motor inhibition during social perception of disgust. Our study suggests an avoidant-defensive mechanism in human cortico-hypoglossal circuits and its 'resonant' activation in the vicarious experience of others' distaste. These findings support a role for the motor system in emotion-driven motor anticipation and social cognition.

Functional Mapping of the Human Auditory Cortex: fMRI Investigation of a Patient with Auditory Agnosia from Trauma to the Inferior Colliculus.

OBJECTIVE: To use functional magnetic resonance imaging to map the auditory cortical fields that are activated, or nonreactive, to sounds in patient M.L., who has auditory agnosia caused by trauma to the inferior colliculi. BACKGROUND: The patient cannot recognize speech or environmental sounds. Her discrimination is greatly facilitated by context and visibility of the speaker's facial movements, and under forced-choice testing. Her auditory temporal resolution is severely compromised. Her discrimination is more impaired for words differing in voice onset time than place of articulation. Words presented to her right ear are extinguished with dichotic presentation; auditory stimuli in the right hemifield are mislocalized to the left. METHODS: We used functional magnetic resonance imaging to examine cortical activations to different categories of meaningful sounds embedded in a block design. RESULTS: Sounds activated the caudal sub-area of M.L.'s primary auditory cortex (hA1) bilaterally and her right posterior superior temporal gyrus (auditory dorsal stream), but not the rostral sub-area (hR) of her primary auditory cortex or the anterior superior temporal gyrus in either hemisphere (auditory ventral stream). CONCLUSIONS: Auditory agnosia reflects dysfunction of the auditory ventral stream. The ventral and dorsal auditory streams are already segregated as early as the primary auditory cortex, with the ventral stream projecting from hR and the dorsal stream from hA1. M.L.'s leftward localization bias, preserved audiovisual integration, and phoneme perception are explained by preserved processing in her right auditory dorsal stream.

Connectivity between the superior colliculus and the amygdala in humans and macaque monkeys: virtual dissection with probabilistic DTI tractography.

It has been suggested that some cortically blind patients can process the emotional valence of visual stimuli via a fast, subcortical pathway from the superior colliculus (SC) that reaches the amygdala via the pulvinar. We provide in vivo evidence for connectivity between the SC and the amygdala via the pulvinar in both humans and rhesus macaques. Probabilistic diffusion tensor imaging tractography revealed a streamlined path that passes dorsolaterally through the pulvinar before arcing rostrally to traverse above the temporal horn of the lateral ventricle and connect to the lateral amygdala. To obviate artifactual connectivity with crossing fibers of the stria terminalis, the stria was also dissected. The putative streamline between the SC and amygdala traverses above the temporal horn dorsal to the stria terminalis and is positioned medial to it in humans and lateral to it in monkeys. The topography of the streamline was examined in relation to lesion anatomy in five patients who had previously participated in behavioral experiments studying the processing of emotionally valenced visual stimuli. The pulvinar lesion interrupted the streamline in two patients who had exhibited contralesional processing deficits and spared the streamline in three patients who had no deficit. Although not definitive, this evidence supports the existence of a subcortical pathway linking the SC with the amygdala in primates. It also provides a necessary bridge between behavioral data obtained in future studies of neurological patients, and any forthcoming evidence from more invasive techniques, such as anatomical tracing studies and electrophysiological investigations only possible in nonhuman species.