Neurons in primate prefrontal cortex signal valuable social information during natural viewing.

Information about social partners is innately valuable to primates. Decisions about which sources of information to consume are highly naturalistic but also complex and place unusually strong demands on the brain's decision network. In particular, both the orbitofrontal cortex (OFC) and lateral prefrontal cortex (LPFC) play key roles in decision making and social behaviour, suggesting a likely role in social information-seeking as well. To test this idea, we developed a 'channel surfing' task in which monkeys were shown a series of 5 s video clips of conspecifics engaged in natural behaviours at a field site. Videos were annotated frame-by-frame using an ethogram of species-typical behaviours, an important source of social information. Between each clip, monkeys were presented with a choice between targets that determined which clip would be seen next. Monkeys' gaze during playback indicated differential engagement depending on what behaviours were presented. Neurons in both OFC and LPFC responded to choice targets and to video, and discriminated a subset of the behaviours in the ethogram during video viewing. These findings suggest that both OFC and LPFC are engaged in processing social information that is used to guide dynamic information-seeking decisions. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Neuronal correlates of strategic cooperation in monkeys.

We recorded neural activity in male monkeys playing a variant of the game 'chicken' in which they made decisions to cooperate or not cooperate to obtain rewards of different sizes. Neurons in the middle superior temporal sulcus (mSTS)-previously implicated in social perception-signaled strategic information, including payoffs, intentions of the other player, reward outcomes and predictions about the other player. Moreover, a subpopulation of mSTS neurons selectively signaled cooperatively obtained rewards. Neurons in the anterior cingulate gyrus, previously implicated in vicarious reinforcement and empathy, carried less information about strategic variables, especially cooperative reward. Strategic signals were not reducible to perceptual information about the other player or motor contingencies. These findings suggest that the capacity to compute models of other agents has deep roots in the strategic social behavior of primates and that the anterior cingulate gyrus and the mSTS support these computations.

Object comparison in the lateral intraparietal area.

We can search for and locate specific objects in our environment by looking for objects with similar features. Object recognition involves stimulus similarity responses in ventral visual areas and task-related responses in prefrontal cortex. We tested whether neurons in the lateral intraparietal area (LIP) of posterior parietal cortex could form an intermediary representation, collating information from object-specific similarity map representations to allow general decisions about whether a stimulus matches the object being looked for. We hypothesized that responses to stimuli would correlate with how similar they are to a sample stimulus. When animals compared two peripheral stimuli to a sample at their fovea, the response to the matching stimulus was similar, independent of the sample identity, but the response to the nonmatch depended on how similar it was to the sample: the more similar, the greater the response to the nonmatch stimulus. These results could not be explained by task difficulty or confidence. We propose that LIP uses its known mechanistic properties to integrate incoming visual information, including that from the ventral stream about object identity, to create a dynamic representation that is concise, low dimensional, and task relevant and that signifies the choice priorities in mental matching behavior.NEW & NOTEWORTHY Studies in object recognition have focused on the ventral stream, in which neurons respond as a function of how similar a stimulus is to their preferred stimulus, and on prefrontal cortex, where neurons indicate which stimulus is being looked for. We found that parietal area LIP uses its known mechanistic properties to form an intermediary representation in this process. This creates a perceptual similarity map that can be used to guide decisions in prefrontal areas.

A lack of anticipatory remapping of retinotopic receptive fields in the middle temporal area.

The middle temporal (MT) area has traditionally been thought to be a retinotopic area. However, recent functional magnetic resonance imaging and psychophysical evidence have suggested that human MT may have some spatiotopic processing. To gain an understanding of the neural mechanisms underlying this process, we recorded neurons from area MT in awake behaving animals performing a simple saccade task in which a spatially stable moving dot stimulus was presented for 500 ms in one of two locations: the presaccadic receptive field or the postsaccadic receptive field. MT neurons responded as if their receptive fields were purely retinotopic. When the stimulus was placed in the presaccadic receptive field, the response was elevated until the saccade took the stimulus out of the receptive field. When the stimulus was placed in the postsaccadic receptive field, the neuron only began its response after the end of the saccade. No evidence of presaccadic or anticipatory remapping was found. We conclude that gain fields are most likely to be responsible for the spatiotopic signal seen in area MT.

Microstimulation of posterior parietal cortex biases the selection of eye movement goals during search.

People can find objects in a visual scene fast and effortlessly. It is thought that this may be accomplished by creating a map of the outside world that incorporates bottom-up sensory and top-down cognitive inputs--a priority map. Eye movements are made toward the location represented by the highest activity on the priority map. We hypothesized that the lateral intraparietal area (LIP) of posterior parietal cortex acts as such a map. To test this, we performed low current microstimulation on animals trained to perform a foraging task and asked whether we could bias the animals to make a saccade to a particular stimulus, by creating an artificial peak of activity at the location representing that stimulus on the map. We found that microstimulation slightly biased the animals to make saccades to visual stimuli at the stimulated location, without actively generating saccades. The magnitude of this effect was small, but it appeared to be similar for all visual stimuli. We interpret these results to mean that microstimulation slightly biased saccade goal selection to the object represented at the stimulated location in LIP.

Been there, seen that: a neural mechanism for performing efficient visual search.

In everyday life, we efficiently find objects in the world by moving our gaze from one location to another. The efficiency of this process is brought about by ignoring items that are dissimilar to the target and remembering which target-like items have already been examined. We trained two animals on a visual foraging task in which they had to find a reward-loaded target among five task-irrelevant distractors and five potential targets. We found that both animals performed the task efficiently, ignoring the distractors and rarely examining a particular target twice. We recorded the single unit activity of 54 neurons in the lateral intraparietal area (LIP) while the animals performed the task. The responses of the neurons differentiated between targets and distractors throughout the trial. Further, the responses marked off targets that had been fixated by a reduction in activity. This reduction acted like inhibition of return in saliency map models; items that had been fixated would no longer be represented by high enough activity to draw an eye movement. This reduction could also be seen as a correlate of reward expectancy; after a target had been identified as not containing the reward the activity was reduced. Within a trial, responses to the remaining targets did not increase as they became more likely to yield a result, suggesting that only activity related to an event is updated on a moment-by-moment bases. Together, our data show that all the neural activity required to guide efficient search is present in LIP. Because LIP activity is known to correlate with saccade goal selection, we propose that LIP plays a significant role in the guidance of efficient visual search.

Psychophysical evidence for spatiotopic processing in area MT in a short-term memory for motion task.

The middle temporal (MT) area has long been established as a cortical area involved in the encoding of motion information and has been thought to do so in retinotopic coordinates. It was previously shown that memory for motion has a spatial component by demonstrating that subjects do significantly worse on a match-to-sample task when the stimuli to be compared were spatially separated. The distance at which performance deteriorated (the critical spatial separation) increased at increasing eccentricities, suggesting that area MT was involved in the process. In this study, we asked whether optimal performance occurred when the stimuli were in the same retinotopic or spatiotopic coordinates. We found that the performance was best when the stimuli appeared in the same location in space rather than the same retinal location, after an eye movement. We also found that the relationship between retinal eccentricity and the critical spatial separation approximated that of area MT, as found previously. We conclude that area MT plays an important role in the memory for motion process and that this is carried out in spatiotopic coordinates. This conclusion supports the hypothesis that MT processing may have a spatiotopic component.