Vivian M. Ciaramitaro

Selectivity for the configural cues that identify the gender, ethnicity, and identity of faces in human cortex

We used psychophysical and functional MRI (fMRI) adaptation to examine how and where the visual configural cues underlying identification of facial ethnicity, gender, and identity are processed. We found that the cortical regions showing selectivity to these cues are distributed widely across the inferior occipital cortex, fusiform areas, and the cingulate gyrus. These regions were not colocalized with areas activated by traditional face area localizer scans. Traditional face area localizer scans isolate regions defined by stronger fMRI responses to a random series of face images than to a series of non-face images. Because these scans present a random assortment of face images, they presumably produce the strongest responses within regions containing neurons that are face-sensitive but not highly tuned for face type. These areas might be expected to show only weak selective adaptation effects. In contrast, the largest responses to our selective adaptation paradigm would be expected within areas containing more selectively tuned neurons that might be expected to show only a sparse collective response to a series of random faces. Many aspects of face processing (e.g., prosopagnosia, recognition, and configural vs. featural processing) are likely to rely heavily on regions containing high proportions of neurons that show selective tuning for faces.

Effects of feature-based attention on the motion aftereffect at remote locations.

Previous studies have shown that attention to a particular stimulus feature, such as direction of motion or color, enhances neuronal responses to unattended stimuli sharing that feature. We studied this effect psychophysically by measuring the strength of the motion aftereffect (MAE) induced by an unattended stimulus when attention was directed to one of two overlapping fields of moving dots in a different spatial location. When attention was directed to the same direction of motion as the unattended stimulus, the unattended stimulus induced a stronger MAE than when attention was directed to the opposite direction. Also, when the unattended location contained either uncorrelated motion or had no stimulus at all an MAE was induced in the opposite direction to the attended direction of motion. The strength of the MAE was similar regardless of whether subjects attended to the speed or luminance of the attended dots. These results provide further support for a global feature-based mechanism of attention, and show that the effect spreads across all features of an attended object, and to all locations of visual space.

Stimulus probability directs spatial attention: an enhancement of sensitivity in humans and monkeys

We examined whether improvements in sensory processing, defined as changes in sensitivity, could be elicited in a simple luminance discrimination task without eliciting concomitant changes in decision processing. To this end we developed a task, for use in both humans and monkeys, in which prior knowledge about where a discriminative stimulus was likely to appear (1) offered no decisional advantage in solving our task and (2) could be parametrically varied to yield a psychometric function. We found that if we parametrically varied the quality of prior knowledge, by increasing the probability, and thus the certainty, that a discriminative stimulus would appear at a particular location under these conditions, luminance discrimination improved for both human and monkey subjects. This improvement was correlated with an enhancement in sensory processing, but not with any systematic changes in decisional processing, as assessed by signal detection theory. These results suggest that (1) sensory processing and decision processing can be separated by task design and (2) systematic changes in prior knowledge about where a stimulus may appear can lead to systematic changes in sensitivity; providing a psychometric function for the influence of prior knowledge on perceptual sensitivity. Importantly, these results were obtained from both human and monkey subjects. Similar task designs could be used in physiological studies attempting to generate linking hypotheses between psychometric and neurometric functions, ultimately allowing changes in perceptual sensitivity to be linked to changes in an underlying neural substrate.

Application of neurosonography to experimental physiology

When Horsley and Clark invented the stereotaxic technique they revolutionized experimental neurobiology. For the first time it became possible to repeatably place experimental or surgical probes at precise locations within the skull. Unfortunately, variations in the position and size of neuroanatomical structures within the cranium have always limited the efficiency of this technology. Recent advances in diagnostic medical ultrasonography, however, allow for the real-time visualization of anatomical structures, in some cases with resolutions of up to 150 microm. We report here that commercially available ultrasonographs can be used in the laboratory to generate real-time in vivo images of brain structures in both anesthetized and awake-behaving animals. We found that ultrasonic imaging is compatible with many types of experimental probes including single neuron recording electrodes, microinjection pipettes, and electrodes for producing electrolytic lesions. Ultrasonic imaging can be used to place, monitor and visualize these probes in vivo. In our hands, commercially available ultrasonic probes designed for pediatric use allowed us to visualize anatomical structures with sub-millimeter resolution in primate brains. Finally, ultrasonic imaging allowed us to reduce the risk of accidentally damaging major blood vessels, greatly reducing the incidence of stroke as an unintended complication of an experimental neurosurgical procedure. Diagnostic ultrasound holds the promise of reducing the uncertainty associated with stereotaxic surgery, an improvement which would significantly improve the efficiency of many neurobiological investigations, reducing the number of animal subjects employed in this research. While this demonstration focuses on sonographic imaging in non-human primates, similar advances should also be possible for studies in other species, including rodents.

Disinhibition of the Superior Colliculus Restores Orienting to Visual Stimuli in the Hemianopic Field of the Cat

Following unilateral removal of all known visual cortical areas, a cat is rendered hemianopic in the contralateral visual field. Visual orientation can be restored to the blind hemifield by transection of the commissure of the superior colliculus or by destruction of the superior colliculus (SC) or the substantia nigra pars reticulata (SNpr) contralateral to the cortical lesion. It is hypothesized that a mechanism mediating recovery is disinhibition of the SC ipsilateral to the cortical lesion. The ipsilateral nigrotectal projection exerts a robust inhibitory tone onto cells in the SC. However, ibotenic acid destruction of SNpr neurons, which should decrease inhibition onto the SC, does not result in recovery. The failure of ipsilateral SNpr lesions to produce recovery puts into question the validity of SC disinhibition as a mechanism of recovery. We directly tested the disinhibition hypothesis by reversibly disinhibiting the SC ipsilateral to a visual cortical lesion with a gamma‐aminobutyric acid (GABA)A antagonist, bicuculline methiodide. In accordance with the hypothesis, transient disinhibition of the SC restored visual orienting for several hours in three of eight animals. Recovery was not a volume or pH effect and was distinct from the release of irrepressible motor effects (i.e., approach and avoidance behaviors) seen within the first hour after injection. Thus, in the absence of all visual cortical areas unilaterally, disinhibition of the SC can transiently restore the ability of the cat to orient to visual stimuli in the previously “blind” hemifield. J. Comp. Neurol. 387:568–587, 1997.

Ibotenic acid lesions of the substantia nigra pars reticulata ipsilateral to a visual cortical lesion fail to restore visual orienting responses in the cat

Unilateral removal of all known visual cortical areas in the cat renders the animal hemianopic in the contralateral visual field as measured by visual perimetry and other behavioral tests. We have shown that visual orientation behavior can be restored to the previously blind hemifield by destruction of a critical zone in the substantia nigra pars reticulata contralateral to a cortical lesion (Wallace et al., J. Comp. Neurol. 296:222–252, 1990). The model proposed to explain this recovery postulates that damage to the crossed nigrotectal projection disinhibits the superior colliculus ipsilateral to the cortical lesion and this leads to recovery. If disinhibition can account for recovery, then destruction of the uncrossed nigrotectal projection, which is known to exert a tonic inhibition on the superior colliculus, should also result in recovery.

Visual detection deficits following inactivation of the superior colliculus in the cat

Lesion or inactivation of the superior colliculus (SC) of the cat results in an animal that fails to orient toward peripheral visual stimuli which normally evoke a brisk, reflexive orienting response. A failure to orient toward a visual stimulus could be the result of a sensory impairment (a failure to detect the visual stimulus) or a motor impairment (an inability to generate the orienting response). Either mechanism could explain the deficit observed during SC inactivation since neurons in the SC can carry visual sensory signals as well as motor commands involved in the generation of head and eye movements. We investigated the effects of SC inactivation in the cat in two ways. First, we tested cats in a visual detection task that required the animals to press a central, stationary foot pedal to indicate detection of a peripheral visual stimulus. Such a motor response does not involve any components of the orienting response and is unlikely to depend on SC motor commands. A deficit in this task would indicate that the SC plays an important role in the detection of visual targets even in a task that does not require visual orienting. Second, to further investigate the visual orienting deficit observed during SC inactivation and to make direct comparisons between detection and orienting performance, we tested cats in a standard perimetry paradigm. Performance in both tasks was tested following focal inactivation of the SC with microinjections of muscimol at various depths and rostral/caudal locations throughout the SC. Our results reveal a dramatic deficit in both the visual detection task and the visual orienting task following inactivation of the SC with muscimol.

Interdependent mechanisms for processing gender and emotion: The special status of angry male faces

While some models of how various attributes of a face are processed have posited that face features, invariant physical cues such as gender or ethnicity as well as variant social cues such as emotion, may be processed independently (e.g., Bruce and Young, 1986), other models suggest a more distributed representation and interdependent processing (e.g., Haxby et al., 2000). Here, we use a contingent adaptation paradigm to investigate if mechanisms for processing the gender and emotion of a face are interdependent and symmetric across the happy–angry emotional continuum and regardless of the gender of the face. We simultaneously adapted participants to angry female faces and happy male faces (Experiment 1) or to happy female faces and angry male faces (Experiment 2). In Experiment 1, we found evidence for contingent adaptation, with simultaneous aftereffects in opposite directions: male faces were biased toward angry while female faces were biased toward happy. Interestingly, in the complementary Experiment 2, we did not find evidence for contingent adaptation, with both male and female faces biased toward angry. Our results highlight that evidence for contingent adaptation and the underlying interdependent face processing mechanisms that would allow for contingent adaptation may only be evident for certain combinations of face features. Such limits may be especially important in the case of social cues given how maladaptive it may be to stop responding to threatening information, with male angry faces considered to be the most threatening. The underlying neuronal mechanisms that could account for such asymmetric effects in contingent adaptation remain to be elucidated.

What's in a Face? How Face Gender and Current Affect Influence Perceived Emotion

Faces drive our social interactions. A vast literature suggests an interaction between gender and emotional face perception, with studies using different methodologies demonstrating that the gender of a face can affect how emotions are processed. However, how different is our perception of affective male and female faces? Furthermore, how does our current affective state when viewing faces influence our perceptual biases? We presented participants with a series of faces morphed along an emotional continuum from happy to angry. Participants judged each face morph as either happy or angry. We determined each participant’s unique emotional ‘neutral’ point, defined as the face morph judged to be perceived equally happy and angry, separately for male and female faces. We also assessed how current state affect influenced these perceptual neutral points. Our results indicate that, for both male and female participants, the emotional neutral point for male faces is perceptually biased to be happier than for female faces. This bias suggests that more happiness is required to perceive a male face as emotionally neutral, i.e., we are biased to perceive a male face as more negative. Interestingly, we also find that perceptual biases in perceiving female faces are correlated with current mood, such that positive state affect correlates with perceiving female faces as happier, while we find no significant correlation between negative state affect and the perception of facial emotion. Furthermore, we find reaction time biases, with slower responses for angry male faces compared to angry female faces.

The Strength of Adaptation to Negative versus Positive Emotional Information Depends on Social Anxiety Status

CONCLUSIONS: § Negative Affect and face gender may account for differences in baseline bias with social anxiety. § Adaptation is weaker for negative vs positive emotions in socially anxious individuals, and weaker for angry male faces vs angry female faces. Sample References: Heimberg, R. G., Brozovich, F. A., & Rapee, R. M. (2014). A cognitivebehavioral model of social anxiety disorder. In S. G. Hofmann, & P. M. DiBartolo (Eds.), Social anxiety: Clinical, developmental, and social perspectives (pp. 705–728) (3rd ed.). Waltham, MA: Academic Press. Yoon, K. L., & Zinbarg, R. E. (2007). Threat is in the eye of the beholder: Social anxiety and the interpretation of ambiguous facial expressions. Behaviour Research and Therapy, 45(4), 839-847.