Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex.

In the previous paper the locations and basic response properties of N200 and other face-specific event-related potentials (ERPs) were described. In this paper responsiveness of N200 and related ERPs to the perceptual features of faces and other images was assessed. N200 amplitude did not vary substantially, whether evoked by colored or grayscale faces; normal, blurred or line-drawing faces; or by faces of different sizes. Human hands evoked small N200s at face-specific sites, but evoked hand-specific ERPs at other sites. Cat and dog faces evoked N200s that were 73% as large as to human faces. Hemifield stimulation demonstrated that the right hemisphere is better at processing information about upright faces and transferring it to the left hemisphere, whereas the left hemisphere is better at processing information about inverted faces and transferring it to the right hemisphere. N200 amplitude was largest to full faces and decreased progressively to eyes, face contours, lips and noses viewed in isolation. A region just lateral to face-specific N200 sites was more responsive to internal face parts than to faces, and some sites in ventral occipitotemporal cortex were face-part-specific. Faces with eyes averted or closed evoked larger N200s than those evoked by faces with eyes forward. N200 amplitude and latency were affected by the joint effects of eye and head position in the right but not in the left hemisphere. Full and three-quarter views of faces evoked larger N200s than did profile views. The results are discussed in relation to behavioral studies in humans and single-cell recordings in monkeys.     

Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials.

This is the last in a series of papers dealing with intracranial event-related potential (ERP) correlates of face perception. Here we describe the results of manipulations that may exert top-down influences on face recognition and face-specific ERPs, and the effects of cortical stimulation at face-specific sites. Ventral face-specific N200 was not evoked by affective stimuli; showed little or no habituation; was not affected by the familiarity or unfamiliarity of faces; showed no semantic priming; and was not affected by face-name learning or identification. P290 and N700 were affected by semantic priming and by face-name learning and identification. The early fraction of N700 and face-specific P350 exhibited significant habituation. About half of the AP350 sites exhibited semantic priming, whereas the VP350 and LP350 sites did not. Cortical stimulation evoked a transient inability to name familiar faces or evoked face-related hallucinations at two-thirds of face-specific N200 sites. These results are discussed in relation to human behavioral studies and monkey single-cell recordings. Discussion of results of all three papers concludes that: face-specific N200 reflects the operation of a module specialized for the perception of human faces; ventral and lateral occipitotemporal cortex are composed of a complex mosaic of functionally discrete patches of cortex of variable number, size and location; in ventral cortex there is a posterior-to-anterior trend in the location of patches in the order letter-strings, form, hands, objects, faces and face parts; P290 and N700 at face-specific N200 sites, and face-specific P350, are subject to top-down influences.     

Electrophysiological and haemodynamic correlates of face perception,recognition and priming

Face perception, recognition and priming were examined with event-related functional magnetic resonance imaging (fMRI) and scalp event-related potentials (ERPs). Face perception was associated with haemodynamic increases in regions including bilateral fusiform and right superior temporal cortices, and a right posterior negativity (N170), most likely generated in the superior temporal region. Face recognition was associated with haemodynamic increases in fusiform, medial frontal and orbitofrontal cortices, and with a frontocentral positivity from 550 ms poststimulus. Face repetition was associated with a positivity from 400 to 600 ms and behavioural priming. Repetition of familiar faces was also associated with earlier onset of the ERP familiarity effect, and haemodynamic decreases in fusiform cortex. These data support a multi-component model of face-processing, with priming arising from more than one stage.     

The timing of perceptual decisions for ambiguous face stimuli in the human ventral visual cortex

When observers must discriminate a weak sensory signal in noise, early sensory areas seem to reflect the instantaneous strength of the sensory signal. In contrast, high-level parietal and prefrontal areas appear to integrate these signals over time with activity peaking at the time of the observer's decision. Here, we used functional magnetic resonance imaging to investigate how the brain forms perceptual decisions about complex visual forms in a challenging task, requiring the discrimination of ambiguous 2-tone Mooney faces and visually similar nonface images. Face-selective areas in the ventral visual cortex showed greater activity when subjects reported perceiving a face as compared with a nonface, even on error trials. More important, activity was closely related to the time of the subject's decision for face judgments, even on individual trials, and resembled the time course of activity in motor cortex corresponding to the subject's behavioral report. These results indicate that perceptual decisions about ambiguous face-like stimuli are reflected early in the sensorimotor pathway, in face-selective regions of the ventral visual cortex. Activity in these areas may represent a potential rate-limiting step in the pathway from sensation to action when subjects must reach a decision about ambiguous face-like stimuli.     

Activation of the human occipital and parietal cortex by pattern and luminance stimuli: neuromagnetic measurements

We compared cortical reactivity to pattern and luminance stimuli by recording evoked responses and spontaneous brain rhythms from 10 subjects with a whole-scalp neuromagnetometer. Hemifield patterns (black-and-white checkerboards) elicited strong contralateral transient activation of the occipital V1/V2 cortex, maximum at 65-75 ms, followed by sustained activation during the 2 s stimulus. Responses to hemifield luminance stimuli also had an occipital component, but they were dominated by activation of the medial parieto-occipital sulcus (POS) 60- 70 ms later. The POS region was equally well activated by foveal and extrafoveal stimuli. The occipital responses to hemifield luminance stimuli differed from those to pattern stimuli in two main aspects: the sustained activation was significantly weaker, and the responses were almost symmetrical, indicating a surprisingly bilateral occipital activation. These effects were similar with foveal and extrafoveal stimuli. The spontaneous 10 Hz alpha rhythm, originating predominantly in the POS region, was suppressed after both stimulus onsets and offsets, more strongly for luminance than pattern stimuli. Activation of the occipital cortex dominated after pattern stimuli, whereas the effect of luminance stimulation was stronger in the parieto-occipital region. The distinct signal distributions in the occipital and POS regions suggest that the two types of stimuli activate the magno- and parvocellular pathways to a varying degree. These findings are also in line with a stronger attention-catching value of the luminance than pattern stimuli.      

An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex.

Studies of patients with cerebral achromatopsia have suggested that ventral occipitotemporal cortex is important for color perception. We created a functional magnetic resonance imaging (fMRI) version of a clinical test commonly used to assess achromatopsia, the Farnsworth-Munsell 100-Hue test. The test required normal subjects to use color information in the visual stimulus to perform a color sequencing task. A modification of the test requiring ordering by luminance was used as a control task. Subjects were also imaged as they passively viewed colored stimuli. A limited number of areas responded more to chromatic than achromatic stimulation, including primary visual cortex. Most color-selective activity was concentrated in ventral occipitotemporal cortex. Several areas in ventral cortex were identified. The most posterior, located in posterior fusiform gyrus, corresponded to the area activated by passive viewing of colored stimuli. More anterior and medial color-selective areas were located in the collateral sulcus and fusiform gyrus. These more anterior areas were not identified in previous imaging studies which used passive viewing of colored stimuli, and were most active in our study when visual color information was behaviorally relevant, suggesting that attention influences activity in color-selective areas. The fMRI version of the Farnsworth-Munsell test may be useful in the study of achromatopsia.     

Categorical perception of somesthetic stimuli: psychophysical measurements correlated with neuronal events in primate medial premotor cortex

In this paper we describe a type of neuron of the medial premotor cortex (MPC) that discharged differentially during a categorization task and reflected in their activity whether the speed of a tactile stimulus was low or high. The activity of these neurons was recorded in the MPC contralateral (right MPC, n = 88) and ipsilateral (left MPC, n = 103) to the stimulated hand of four monkeys performing this somesthetic task. Animals performed the task by pressing with the right hand one of two target switches to indicate whether the speed of probe movement across the skin of the left hand was low or high. Differential responses of MPC neurons occurred during the stimulus and reaction time period. We used an analysis based on signal detection theory to determine whether these differential responses were associated with the animal's decision. According to this analysis, 104 of the 191 neurons (right MPC, n = 48; left MPC, n = 56) coded the categorization of the stimulus speeds (categorical neurons). In a light instruction task, we tested the possibility that the categorical neurons (n = 71) were associated with the intention to press, or with the trajectory of the hand to one of the two target switches used to indicate categorization. In this situation, each trial began as in the somesthetic categorization task, but one of the two target switches was illuminated beginning with the skin indentation, continued during the delay period and turned off when the probe was lifted off from the skin. This condition instructed the animal which target switch was required to be pressed for reward. Very few neurons (14 of 71) maintained their differential responses observed in the categorization task. Some categorical neurons (n = 5) were also studied; the animal categorized the tactile stimulus speeds, but knew in advance whether the stimulus speed was low or high (categorization + light instruction). This was made by illuminating one of the two target switches which was associated with the stimulus speed. The categorical response was considerably attenuated in this condition. Interestingly, during the delay period, these neurons reflected in their activity whether the stimulus was low or high. A number of the categorical MPC neurons (n = 30) were studied when the same set of stimuli, used in the categorization, were delivered passively. None of these neurons responded in this condition. These results suggest that the MPC, apart from its well-known role in motor behavior, is also involved in the animal's decision during the execution of this learned somesthetic task.      

Amplitude and frequency-modulated stimuli activate common regions of human auditory cortex

Hall et al. (Hall et al., 2002, Cerebral Cortex 12:140-149) recently showed that pulsed frequency-modulated tones generate considerably higher activation than their unmodulated counterparts in non-primary auditory regions immediately posterior and lateral to Heschl's gyrus (HG). Here, we use fMRI to explore the type of modulation necessary to evoke such differential activation. Carrier signals were a single tone and a harmonic-complex tone, with a 300 Hz fundamental, that were modulated at a rate of 5 Hz either in frequency, or in amplitude, to create six stimulus conditions (unmodulated, FM, AM). Relative to the silent baseline, the modulated tones, in particular, activated widespread regions of the auditory cortex bilaterally along the supra-temporal plane. When compared with the unmodulated tones, both AM and FM tones generated significantly greater activation in lateral HG and the planum temporale, replicating the previous findings. These activation patterns were largely overlapping, indicating a common sensitivity to both AM and FM. Direct comparisons between AM and FM revealed a higher magnitude of activation in response to the variation in amplitude than in frequency, plus a small part of the posterolateral region in the right hemisphere whose response was specifically AM-, and not FM-, dependent. The dominant pattern of activation was that of co-localized activation by AM and FM, which is consistent with a common neural code for AM and FM within these brain regions.     

Duration-dependent FMRI adaptation and distributed viewer-centered face representation in human visual cortex

Two functional magnetic resonance imaging (fMRI) face viewpoint adaptation experiments were conducted to investigate whether fMRI adaptation in high-level visual cortex depends on the duration of adaptation and how different views of a face are represented in the human visual system. We found adaptation effects in multiple face-selective areas, which suggest a distributed, viewer-centered representation of faces in the human visual system. However, the nature of the adaptation effects was dependent on the length of adaptation. With long adaptation durations, face-selective areas along the hierarchy of the visual system gradually exhibited viewpoint-tuned adaptation. As the angular difference between the adapter and test stimulus increased, the blood oxygen level-dependent (BOLD) signal evoked by the test stimulus gradually increased as a function of the amount of 3-dimensional (3D) rotation. With short adaptation durations, however, face-selective areas in the ventral pathway, including the lateral occipital cortex and right fusiform area, exhibited viewpoint-sensitive adaptation. These areas showed an increase in the BOLD signal with a 3D rotation, but this signal increase was independent of the amount of rotation. Further, the right superior temporal sulcus showed little or very weak viewpoint adaptation with short adaptation durations. Our findings suggest that long- and short-term fMRI adaptations may reflect selective properties of different neuronal mechanisms.     

Cochlear nerve injuries caused by manipulations in cerebellopontine angle: Part I. Electrophysiological and morphological study in dogs

Cochlear nerve injuries caused by manipulations in the cerebellopontine angle were electrophysiologically and morphologically investigated using dogs. Compression injuries were developed at the portions of the cochlear nerves that were directly retracted by a retractor. The blood vessels supplying the cochlear nerve trunk easily ruptured and the Schwann-glial junctions of the cochlear nerve were separated, due to traction force derived from the manipulations in the CP angle. From these results, some technical points to preserve hearing during CP angle surgery were discussed.     

Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study.

In order to determine the electrophysiological properties of prefrontal cortex pyramidal neurons in vivo, intracellular recordings coupled with neurobiotin injection were performed in anesthetized rats. Three main classes of pyramidal cells were distinguished according to both their firing patterns in response to depolarizing current pulses and the characteristics of their action potentials: regular spiking (RS, n = 71); intrinsic (inactivating) bursting (IB, n = 8); and non-inactivating bursting (NIB, n = 26) cells. RS cells were further subdivided into slow-adapting and fast-adapting types, according to their firing frequency adaptation. IB and fast-adapting RS cells could exhibit different firing patterns depending on the intensity of the depolarizing current. In response to successive depolarizing pulses of a given intensity, NIB and some RS cells showed variations in their firing patterns, probably due to the impact of local synaptic activity. All the labeled neurons were pyramidal cells with an apical dendrite that formed a terminal tuft in layer I. As compared to RS cells, NIB cells had a smaller somatic size and their apical dendritic tuft was less extensive, while IB cells presented a larger somatic size, thicker dendrites and a wider extent of their basal and apical dendritic arborization. In conclusion, we found in the rat prefrontal cortex, in vivo, different electrophysiological classes of pyramidal cells whose output firing patterns depend on interactions between their intrinsic properties and the ongoing synaptic activity.     

Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies

Recent imaging studies show that the orbitofrontal cortex (OFC) is activated during a wide variety of paradigms, including guessing tasks, simple delayed matching tasks and sentence completion. We suggest that, as with other regions of the prefrontal cortex, activity in the OFC is most likely to be observed when there is insufficient information available to determine the appropriate course of action. In these circumstances the OFC, rather than other prefrontal regions, is more likely to be activated when the problem of what to do next is best solved by taking into account the likely reward value of stimuli and responses, rather than their identity or location. We suggest that selection of stimuli on the basis of their familiarity and responses on the basis of a feeling of 'rightness' are also examples of selection on the basis of reward value. Within the OFC, the lateral regions are more likely to be involved when the action selected requires the suppression of previously rewarded responses.     

Differential regulation by dexamethasone and cyclosporine of human T cells activated by various stimuli.

Calcium ionophores such as ionomycin (IONO), CD3 antibody (CD3), or CD28 antibody (CD28) have been shown to stimulate T cells in a quite different fashion. However, each stimulator induces full activation of resting T cells in the presence of phorbol myristate acetate. Human T cells were activated with PMA + CD3, PMA + IONO, or PMA + CD28 and the inhibitory effects of dexamethasone (DEX) and cyclosporine were examined on [3H]-TdR incorporation, IL-2 production, and IL-2 receptor expression. Three inhibition patterns emerged: PMA + CD3 stimulation was DEX-sensitive and CsA-sensitive, PMA + IONO stimulation was CsA-sensitive but DEX-resistant, PMA + CD28 stimulation was DEX-sensitive but CsA-resistant. Although the degree of inhibition by DEX and CsA was different in [3H] TdR incorporation, IL-2 production, and IL-2 receptor expression assays, the inhibitory pattern of these drugs was similar in each of the assays, indicating that human T cell activation is differentially regulated by DEX and CsA depending on the stimulator.     

Electrophysiological studies of long-term electrical stimulation of the cerebellum in monkeys.

Six rhesus monkeys were stimulated on the paravermal cortex for 205 hours (18 days) with different charge densities in order to determine the electrode performance and neural damage that may result from long-term cerebellar stimulation comparable to that being used in man. The electrode-tissue interface was relatively stable and no neural damage was found when the charge/phase (0.5 muC/ph) or charge density (7.4 muC/sq cm/ph) was very low. At all higher charge levels tested (2.4, 4.8, 10, and 22 muC/ph), changes in the electrode-tissue interface, meningeal encapsulation, and neural damage were directly related to the charge density delivered. Unstimulated electrodes on the opposite paravermal cortex exhibited mild tissue reactivity and cell damage, probably due to mechanical compression of the molecular layer and pial vessels. Motor cortex field potentials could be evoked by charges as low as 0.1 muC/ph delivered to paravermal cortex; for a given charge/phase longer pulses were more effective than short pulses. After neural damage resulting from 205 hours of 4.8 muC pulses at 10 per second (total charge 14.76 C), the threshold for the motor cortex evoked potential increased by a factor of four or more. With the charge held constant to different-sized electrodes placed bilaterally in the same monkey, damage was greater under the smaller electtrode. This finding suggests that the charge density to cerebellar cortex must be controlled to avoid neural damage.