Face processing in different brain areas,and critical band masking

Neurophysiological evidence is described showing that some neurons in the macaque inferior temporal visual cortex have responses that are invariant with respect to the position, size, view, and spatial frequency of faces and objects, and that these neurons show rapid processing and rapid learning. Critical band spatial frequency masking is shown to be a property of these face‐selective neurons and of the human visual perception of faces. Which face or object is present is encoded using a distributed representation in which each neuron conveys independent information in its firing rate, with little information evident in the relative time of firing of different neurons. This ensemble encoding has the advantages of maximizing the information in the representation useful for discrimination between stimuli using a simple weighted sum of the neuronal firing by the receiving neurons, generalization, and graceful degradation. These invariant representations are ideally suited to provide the inputs to brain regions such as the orbitofrontal cortex and amygdala that learn the reinforcement associations of an individual's face, for then the learning, and the appropriate social and emotional responses generalize to other views of the same face. A theory is described of how such invariant representations may be produced by self‐organizing learning in a hierarchically organized set of visual cortical areas with convergent connectivity. The theory utilizes either temporal or spatial continuity with an associative synaptic modification rule. Another population of neurons in the cortex in the superior temporal sulcus encodes other aspects of faces such as face expression, eye‐gaze, face view, and whether the head is moving. These neurons thus provide important additional inputs to parts of the brain such as the orbitofrontal cortex and amygdala that are involved in social communication and emotional behaviour. Outputs of these systems reach the amygdala, in which face‐selective neurons are found, and also the orbitofrontal cortex, in which some neurons are tuned to face identity and others to face expression. In humans, activation of the orbitofrontal cortex is found when a change of face expression acts as a social signal that behaviour should change; and damage to the human orbitofrontal and pregenual cingulate cortex can impair face and voice expression identification, and also the reversal of emotional behaviour that normally occurs when reinforcers are reversed.     

Novel visual stimuli activate a population of neurons in the primate orbitofrontal cortex

Neurons were found in the rhesus macaque anterior orbitofrontal cortex that respond to novel but not to familiar visual stimuli. Some of these neurons responded to all novel stimuli, and others to only a subset (e.g., to novel faces). The neurons have no responses to familiar reward- or punishment-associated visual stimuli, nor to taste, olfactory or somatosensory inputs. The responses of the neurons typically habituated with repeated presentations of a novel stimulus, and five presentations each 1s was the median number for the response to reach half-maximal. The neurons did not respond to stimuli which had been novel and shown a few times on the previous day, indicating that the neurons were involved in long-term memory. The median latency of the neuronal responses was 120 ms. The median spontaneous firing rate was 1.3 spikes/s, and the median response to novel visual stimuli was 6.0 spikes/s. These findings indicate that the long-term memory for visual stimuli is information that is represented in a region of the primate anterior orbitofrontal cortex.     

Top-down control of visual perception: attention in natural vision

Top-down perceptual influences can bias (or pre-empt) perception. In natural scenes, the receptive fields of neurons in the inferior temporal visual cortex (IT) shrink to become close to the size of objects. This facilitates the read-out of information from the ventral visual system, because the information is primarily about the object at the fovea. Top-down attentional influences are much less evident in natural scenes than when objects are shown against blank backgrounds, though are still present. It is suggested that the reduced receptive-field size in natural scenes, and the effects of top-down attention contribute to change blindness. The receptive fields of IT neurons in complex scenes, though including the fovea, are frequently asymmetric around the fovea, and it is proposed that this is the solution the IT uses to represent multiple objects and their relative spatial positions in a scene. Networks that implement probabilistic decision-making are described, and it is suggested that, when in perceptual systems they take decisions (or 'test hypotheses'), they influence lower-level networks to bias visual perception. Finally, it is shown that similar processes extend to systems involved in the processing of emotion-provoking sensory stimuli, in that word-level cognitive states provide top-down biasing that reaches as far down as the orbitofrontal cortex, where, at the first stage of affective representations, olfactory, taste, flavour, and touch processing is biased (or pre-empted) in humans.     

Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions

Currently, many theories highlight either representational memory or rule representation as the hallmark of prefrontal function. Neurophysiological findings in the primate dorsolateral prefrontal cortex indicate that both features may characterize prefrontal processing. Neurons in the dorsolateral prefrontal cortex encode information in working memory, and this information is represented when relevant to the rules governing performance in a task. In this review, we discuss recent reports of encoding in primate and rat orbitofrontal regions indicating that these features also characterize activity in the orbitofrontal subdivision of the prefrontal cortex. These data indicate that (1) neural activity in the orbitofrontal cortex links the current incentive value of reinforcers to cues, rather than representing the physical features of cues or associated reinforcers; (2) this incentive-based information is represented in the orbitofrontal cortex when it is relevant to the rules guiding performance in a task; and (3) incentive information is also represented in the orbitofrontal cortex in working memory during delays when neither the cues nor reinforcers are present. Therefore, although the orbitofrontal cortex appears to be uniquely specialized to process incentive or motivational information, it may be integrated into a more global framework of prefrontal function characterized by representational encoding of performance-relevant information.     

The amygdala and ventromedial prefrontal cortex in morality and psychopathy

Recent work has implicated the amygdala and ventromedial prefrontal cortex in morality and, when dysfunctional, psychopathy. This model proposes that the amygdala, through stimulus-reinforcement learning, enables the association of actions that harm others with the aversive reinforcement of the victims' distress. Consequent information on reinforcement expectancy, fed forward to the ventromedial prefrontal cortex, can guide the healthy individual away from moral transgressions. In psychopathy, dysfunction in these structures means that care-based moral reasoning is compromised and the risk that antisocial behavior is used instrumentally to achieve goals is increased.     

Neural coding of reward magnitude in the orbitofrontal cortex of the rat during a five-odor olfactory discrimination task

The orbitofrontal cortex (OBFc) has been suggested to code the motivational value of environmental stimuli and to use this information for the flexible guidance of goal-directed behavior. To examine whether information regarding reward prediction is quantitatively represented in the rat OBFc, neural activity was recorded during an olfactory discrimination “go”/“no-go” task in which five different odor stimuli were predictive for various amounts of reward or an aversive reinforcer. Neural correlates related to both actual and expected reward magnitude were observed. Responses related to reward expectation occurred during the execution of the behavioral response toward the reward site and within a waiting period prior to reinforcement delivery. About one-half of these neurons demonstrated differential firing toward the different reward sizes. These data provide new and strong evidence that reward expectancy, regardless of reward magnitude, is coded by neurons of the rat OBFc, and are indicative for representation of quantitative information concerning expected reward. Moreover, neural correlates of reward expectancy appear to be distributed across both motor and nonmotor phases of the task.     

Aging affects acquisition and reversal of reward-based associative learning

Reward-based associative learning is mediated by a distributed network of brain regions that are dependent on the dopaminergic system. Age-related changes in key regions of this system, the striatum and the prefrontal cortex, may adversely affect the ability to use reward information for the guidance of behavior. The present study investigated the effects of healthy aging on different components of reward learning, such as acquisition, reversal, effects of reward magnitude, and transfer of learning. A group of 30 young (mean age = 24.2 yr) and a group of 30 older subjects (mean age = 64.1 yr) completed two probabilistic reward-based stimulus association learning tasks. Older subjects showed poorer overall acquisition and impaired reversal learning, as well as deficits in transfer learning. When only those subjects who showed evidence of significant learning were considered, younger subjects showed equivalently fast learning irrespective of reward magnitude, while learning curves in older subjects were steeper for high compared to low reward magnitudes. Acquired equivalence learning, which requires generalization across stimuli and transfer of learned contingencies to new stimuli, was mildly impaired in older subjects.     

Editorial: Information Processing and the Emotional Disorders

Abstract

It is shown that emotions can usefully be considered as states produced by reinforcing stimuli. The ways in which a wide variety of emotions can be produced, and the functions of emotion, are considered. There is evidence that the amygdala is involved in the formation of stimulus-reinforcement associations, and the orbitofrontal cortex with correcting behavioural responses when these are no longer appropriate because previous reinforcement contingencies change. This evidence comes from the effects of damage to these structures, and from recording the activity of single neurons in these structures in the monkey during the formation and disconnection of stimulus-reinforcement associations. In so far as emotions can be defined as states produced by reinforcing stimuli, then the amygdala and orbitofrontal cortex are seen to be of great importance for emotions, in that they are involved respectively in the elicitation of learned emotional responses, and in the correction or adjustment of these emotional responses as the reinforcing value of environmental stimuli alters. One of the theses advanced is that the changes in emotional behaviour produced by damage to the brain can be analysed and understood by considering how different parts of it function in reinforcement and in the formation and disconnection of stimulus-reinforcement connections. Another thesis is that there is a population of neurons in the amygdala and parts of the temporal lobe visual cortex specialised to respond to faces, and that these neurons may be involved in social and emotional resposes to faces.

Some of the outputs of the amygdala and orbitofrontal cortex are directed to the hypothalamus, which not only provides one route for these reinforcing environmental events to produce autonomic responses, but also is implicated in the utilisation of such stimuli in motivational responses, such as feeding and drinking, and in emotional behaviour. Other outputs of the amygdala and orbitofrontal cortex which may enable them to influence behaviour are directed to the striatum, and also back towards some of the cortical regions from which they receive inputs. It is suggested that these latter projections are important in the effects which mood states have on cognitive processing.     

Control of appetitive and aversive taste-reactivity responses by an auditory conditioned stimulus in a devaluation task: a FOS and behavioral analysis

Through associative learning, cues for biologically significant reinforcers such as food may gain access to mental representations of those reinforcers. Here, we used devaluation procedures, behavioral assessment of hedonic taste-reactivity responses, and measurement of immediate-early gene (IEG) expression to show that a cue for food engages behavior and brain activity related to sensory and hedonic processing of that food. Rats first received a tone paired with intraoral infusion of sucrose. Then, in the absence of the tone, the value of sucrose was reduced (Devalue group) by pairing sucrose with lithium chloride (LiCl), or maintained (Maintain group) by presenting sucrose and LiCl unpaired. Finally, taste-reactivity responses to the tone were assessed in the absence of sucrose. Devalue rats showed high levels of aversive responses and minimal appetitive responses, whereas Maintain rats exhibited substantial appetitive responding but little aversive responding. Control rats that had not received tone-sucrose pairings did not display either class of behaviors. Devalue rats showed greater FOS expression than Maintain rats in several brain regions implicated in devaluation task performance and the display of aversive responses, including the basolateral amygdala, orbitofrontal cortex, gustatory cortex (GC), and the posterior accumbens shell (ACBs), whereas the opposite pattern was found in the anterior ACBs. Both Devalue and Maintain rats showed greater FOS expression than control rats in amygdala central nucleus, GC, and both subregions of ACBs. Thus, through associative learning, auditory cues for food gained access to neural processing in several brain regions importantly involved in the processing of taste memory information.     

Involvement of the rat anterior cingulate cortex in control of instrumental responses guided by reward expectancy

The anterior cingulate cortex (ACC) plays a critical role in stimulus-reinforcement learning and reward-guided selection of actions. Here we conducted a series of experiments to further elucidate the role of the ACC in instrumental behavior involving effort-based decision-making and instrumental learning guided by reward-predictive stimuli. In Experiment 1, rats were trained on a cost-benefit T-maze task in which they could either choose to climb a barrier to obtain a high reward (four pellets) in one arm or a low reward (two pellets) in the other with no barrier present. In line with previous studies, our data reveal that rats with quinolinic acid lesions of the ACC selected the response involving less work and smaller reward. Experiment 2 demonstrates that breaking points of instrumental performance under a progressive ratio schedule were similar in sham-lesioned and ACC-lesioned rats. Thus, lesions of the ACC did not interfere with the effort a rat is willing to expend to obtain a specific reward in this test. In a subsequent task, we examined effort-based decision-making in a lever-press task where rats had the choice between pressing a lever to receive preferred food pellets under a progressive ratio schedule, or free feeding on a less preferred food, i.e. lab chow. Results show that sham- and ACC-lesioned animals had similar breaking points and ingested comparable amounts of less-preferred food. Together, the results of Experiment 1 and 2 suggest that the ACC plays a role in evaluating how much effort to expend for reward; however, the ACC is not necessary in all situations requiring an assessment of costs and benefits. In Experiment 3 we investigated learning and reversal learning of instrumental responses guided by reward predictive stimuli. A reaction time (RT) task demanding conditioned lever release was used in which the upcoming reward magnitude (five vs. one food pellet) was signalled in advance by discriminative visual stimuli. Results revealed that rats with ACC lesions were able to discriminate reward magnitude-predictive stimuli and to adapt instrumental behavior to reversed stimulus-reward magnitude contingencies. Thus, in a simple discrimination task as used here, the ACC appears not to be required to discriminate reward magnitude-predictive stimuli and to use the learned significance of the stimuli to guide instrumental behavior.     

物质成瘾及其戒除:基于反转学习的视角

物质成瘾与反转学习损伤密切相关,成瘾者往往不能灵活地适应变化的刺激—结果的联结,这可能进一步加剧成瘾者的物质使用。近年来研究发现,物质成瘾者的反转学习相关的腹外侧前额和背外侧前额等脑区激活异常,这些异常与成瘾者的冲动性和强迫性有关。此外,个体的反转学习能力对其成瘾行为具有一定预测性。今后应增加对不同类型物质成瘾者的反转学习脑机制及物质相关线索对成瘾者反转学习影响的研究,并且进一步探讨成瘾者的冲动性和强迫性对其反转学习的调节及个体反转学习能力对其成瘾行为的预测。     

人脑眶额皮质表征奖赏信息的进展

文章围绕人脑眶额皮质在表征奖赏信息上的核心作用展开,分别从人脑眶额皮质表征奖赏信息的共同神经表征和特异性神经表征特点,奖赏加工和该脑区局部形态特征之间的关系以及眶额皮质表征奖赏信息的时间动态性等角度对最近的重要研究进展进行了一定的梳理和概括。最后,文章讨论了未来研究需要解决的由奖赏类型多样性和脑区间奖赏信息整合复杂性带来的系列问题。     

Somatosensory processes subserving perception and action

The functions of the somatosensory system are multiple. We use tactile input to localize and experience the various qualities of touch, and proprioceptive information to determine the position of different parts of the body with respect to each other, which provides fundamental information for action. Further, tactile exploration of the characteristics of external objects can result in conscious perceptual experience and stimulus or object recognition. Neuroanatomical studies suggest parallel processing as well as serial processing within the cerebral somatosensory system that reflect these separate functions, with one processing stream terminating in the posterior parietal cortex (PPC), and the other terminating in the insula. We suggest that, analogously to the organisation of the visual system, somatosensory processing for the guidance of action can be dissociated from the processing that leads to perception and memory. In addition, we find a second division between tactile information processing about external targets in service of object recognition and tactile information processing related to the body itself. We suggest the posterior parietal cortex subserves both perception and action, whereas the insula principally subserves perceptual recognition and learning.     

Learning blossoms: Caregiver-infant interactions in an outdoor garden setting

Plants provide unique opportunities for learning by engaging all human senses. Recent laboratory studies have shown that infants use a combination of behavioural avoidance and social learning strategies to safely learn about plant properties from adults. Here we investigate how infants and their caregivers interact with plants in an outdoor garden as a first step towards examining the operation of these social learning processes in naturalistic settings. We focus on two specific aspects of spontaneous infant-caregiver interactions with plants: olfactory and touch behaviours. Additionally, we look at whether infants' and caregivers’ prior knowledge of the plants in our study influences infants’ behaviour. Our results showed a multifaceted connection between infants’ and caregivers' previous experience with the plants and their olfactory and touch behaviours. First, infants tended to touch and smell the plants after their caregivers did, and this appeared to be independent of whether infants had seen the plant before. Second, infants systematically engaged in some of the same types of olfactory and touch behaviours their caregiver displayed towards plants. Finally, infants whose caregivers were given more information about the plants in the study showed fewer touch behaviours, but no difference in olfactory behaviours. These findings bolster the previous laboratory studies of plant learning early in life, highlighting the importance of olfactory behaviours, and underscoring the benefits of using ecological observations to explore unique aspects of human development.     

Inferior olive lesions impair concurrent taste aversion learning in rats.

Taste aversion learning can be established according to two different procedures, concurrent and sequential. For the concurrent task, two different taste stimuli are offered at the same time, one associated with simultaneous intragastric administration of an aversive stimulus and the other associated with physiological saline. This discrimination is learned by sham-lesioned control animals and by animals with lesions in the cerebellar cortex but not by rats lesioned in the inferior olive. At the same time, animals with lesions in the inferior olive and sham-lesioned animals achieve sequential learning when the gustatory stimuli are offered individually during each daily session. The results obtained show that electrolytic lesions in the inferior olive impair acquisition of concurrent learning and are analyzed in terms of an anatomical system consisting of the vagus nerve, inferior olive, and cerebellum, which differentiates between the two modalities of taste aversion learning, concurrent and sequential.     

Polysynaptic potentiation at different levels of rat olfactory pathways following learning

This study was aimed at investigating the consequences of learning on late polysynaptic components of evoked field potential signals recorded in parallel at different levels of the olfactory pathways. For this, evoked field potentials induced by electrical stimulation of the olfactory bulb were recorded simultaneously in the anterior piriform cortex, the posterior piriform cortex, the lateral entorhinal cortex, and the dentate gyrus. The different parameters of late components were measured in each site before and after completion of associative learning in anesthetized rats. In the learning task, rats were trained to associate electrical stimulation of one olfactory bulb electrode with the delivery of sucrose (positive reward) and stimulation of a second olfactory bulb electrode with the delivery of quinine (negative reward). In this way, stimulation of the same olfactory bulb electrodes used for inducing field potentials served as a discriminative cue in the learning paradigm. The data confirmed previous observation that learning was associated with a lowering in late-component-1 intensity of induction in the posterior piriform cortex. The use of simultaneous recording allowed us to further specify the consequences of learning on late-component distribution in the studied network. Indeed the data showed that whereas before learning, late component 1 was rather uniformly distributed among the recorded sites; following learning, its expression was facilitated preferentially in the posterior piriform cortex and lateral entorhinal cortex. Furthermore, learning was accompanied by the emergence of a new late component (late component 2), which occurred simultaneously in the four recording sites. The possible involvement of potentiation of polysynaptic components in recognition and/or consolidation processes will be discussed.     

Reward expectation influences audiovisual spatial integration

In order to determine the spatial location of an object that is simultaneously seen and heard, the brain assigns higher weights to the sensory inputs that provide the most reliable information. For example, in the well-known ventriloquism effect, the perceived location of a sound is shifted toward the location of a concurrent but spatially misaligned visual stimulus. This perceptual illusion can be explained by the usually much higher spatial resolution of the visual system as compared to the auditory system. Recently, it has been demonstrated that this cross-modal binding process is not fully automatic, but can be modulated by emotional learning. Here we tested whether cross-modal binding is similarly affected by motivational factors, as exemplified by reward expectancy. Participants received a monetary reward for precise and accurate localization of brief auditory stimuli. Auditory stimuli were accompanied by task-irrelevant, spatially misaligned visual stimuli. Thus, the participants’ motivational goal of maximizing their reward was put in conflict with the spatial bias of auditory localization induced by the ventriloquist situation. Crucially, the amounts of expected reward differed between the two hemifields. As compared to the hemifield associated with a low reward, the ventriloquism effect was reduced in the high-reward hemifield. This finding suggests that reward expectations modulate cross-modal binding processes, possibly mediated via cognitive control mechanisms. The motivational significance of the stimulus material, thus, constitutes an important factor that needs to be considered in the study of top-down influences on multisensory integration.     

Monkey perirhinal cortex is critical for visual memory, but not for visual perception: reexamination of the behavioural evidence from monkeys.

Overdependence on discrimination learning paradigms to assess the function of perirhinal cortex has complicated understanding of the cognitive role of this structure. Impairments in discrimination learning can result from at least two distinct causes: (a) failure to accurately apprehend and represent the relevant stimuli, or (b) failure to form and remember associations between stimulus representations and reward. Thus, the results of discrimination learning experiments do not readily differentiate deficits in perception from deficits in learning and memory. Here I describe studies that do dissociate learning and memory from perception and show that perirhinal cortex damage impairs learning and/or memory, but not perception. Reanalysis and reconsideration of other published data call into further question the hypothesis that the monkey perirhinal cortex plays a critical role in visual perception.     

Monkey perirhinal cortex is critical for visual memory, but not for visual perception: Reexamination of the behavioural evidence from monkeys

Overdependence on discrimination learning paradigms to assess the function of perirhinal cortex has complicated understanding of the cognitive role of this structure. Impairments in discrimination learning can result from at least two distinct causes: (a) failure to accurately apprehend and represent the relevant stimuli, or (b) failure to form and remember associations between stimulus representations and reward. Thus, the results of discrimination learning experiments do not readily differentiate deficits in perception from deficits in learning and memory. Here I describe studies that do dissociate learning and memory from perception and show that perirhinal cortex damage impairs learning and/or memory, but not perception. Reanalysis and reconsideration of other published data call into further question the hypothesis that the monkey perirhinal cortex plays a critical role in visual perception.