Familiarity with visual stimuli boosts recency bias in macaques.

To probe how non-human primates (NHPs) decode temporal dynamic stimuli, we used a two-alternative forced choice task (2AFC), where the cue was dynamic: a movie snippet drawn from an animation that transforms one image into another. When the cue was drawn from either the beginning or end of the animation, thus heavily weighted towards one (the target) of both images (the choice pair), then primates performed at high levels of accuracy. For a subset of trials, however, the cue was ambiguous, drawn from the middle of the animation, containing information that could be associated to either image. Those trials, rewarded randomly and independent of choice, offered an opportunity to study the strategy the animals used trying to decode the cue. Despite being ambiguous, the primates exhibited a clear strategy, suggesting they were not aware that reward was given non-differentially. More specifically, they relied more on information provided at the end than at the beginning of those cues, consistent with the recency effect reported by numerous serial position studies. Interestingly and counterintuitively, this effect became stronger for sessions where the primates were already familiar with the stimuli. In other words, despite having rehearsed with the same stimuli in a previous session, the animals relied even more on a decision strategy that did not yield any benefits during a previous session. In the discussion section we speculate on what might cause this behavioral shift towards stronger bias, as well as why this behavior shows similarities with a repetition bias in humans known as the illusory truth effect.

Detection of spontaneous class-specific visual stimuli with high temporal accuracy in human electrocorticography.

Most brain-computer interface classification experiments from electrical potential recordings have been focused on the identification of classes of stimuli or behavior where the timing of experimental parameters is known or pre-designated. Real world experience, however, is spontaneous, and to this end we describe an experiment predicting the occurrence, timing, and types of visual stimuli perceived by a human subject from electrocorticographic recordings. All 300 of 300 presented stimuli were correctly detected, with a temporal precision of order 20 ms. The type of stimulus (face/house) was correctly identified in 95% of these cases. There were approximately 20 false alarm events, corresponding to a late 2nd neuronal response to a previously identified event.

Time course and stimulus dependence of repetition-induced response suppression in inferotemporal cortex.

Neural responses throughout the sensory system are affected by stimulus history. In the inferotemporal cortex (IT)--an area important for processing information about object shape--there is a substantially reduced response to the second presentation of an image. Understanding the mechanisms underlying repetition suppression may provide important insights into the circuitry that generates responses in IT. In addition, repetition suppression may have important perceptual consequences. The characteristics of repetition suppression in IT are poorly understood, and the details, including the interaction between the content of the first and second stimulus and the time course of suppression, are not clear. Here, we examined the time course of suppression in IT by varying both the duration and stimulus content of two stimuli presented in sequence. The data show that the degree of suppression does not depend directly on the response evoked by the first stimulus in the recorded neuron. Repetition suppression was also limited in duration, peaking at approximately 200 ms after the onset of the second (test) image and disappearing before the end of the response. Neural selectivity to a continuum of related images was enhanced if the first stimulus produced a weak response in the cell. The dynamics of the response suggests that different parts of the input and recurrent circuitry that gives rise to neural responses in IT are differentially modulated by repetition suppression. The selectivity of the sustained response was preserved in spite of substantial suppression of the early part of the response. The data suggest that suppression in IT is a property of the input and recurrent circuitry in IT and is not directly related to the degree of response in the recorded neuron itself.

Converging neuronal activity in inferior temporal cortex during the classification of morphed stimuli.

How does the brain dynamically convert incoming sensory data into a representation useful for classification? Neurons in inferior temporal (IT) cortex are selective for complex visual stimuli, but their response dynamics during perceptual classification is not well understood. We studied IT dynamics in monkeys performing a classification task. The monkeys were shown visual stimuli that were morphed (interpolated) between pairs of familiar images. Their ability to classify the morphed images depended systematically on the degree of morph. IT neurons were selected that responded more strongly to one of the 2 familiar images (the effective image). The responses tended to peak approximately 120 ms following stimulus onset with an amplitude that depended almost linearly on the degree of morph. The responses then declined, but remained above baseline for several hundred ms. This sustained component remained linearly dependent on morph level for stimuli more similar to the ineffective image but progressively converged to a single response profile, independent of morph level, for stimuli more similar to the effective image. Thus, these neurons represented the dynamic conversion of graded sensory information into a task-relevant classification. Computational models suggest that these dynamics could be produced by attractor states and firing rate adaptation within the population of IT neurons.

Modulation of neural responses in inferotemporal cortex during the interpretation of ambiguous photographs.

Ambiguous images are interpreted in the context of biases about what they might be; these biases and the behavioral consequences induced by them may influence the processing of images. In this report, we examine neural responses in inferotemporal cortex (IT) during the interpretation of ambiguous photographs created by morphing between two photographs. Monkeys classified different images as being one of two choices and learned to classify most of the samples correctly. For one image (the ambiguous sample) reward was administered randomly for either possible choice, and the monkeys were free to classify that image based on their own interpretation, with no learning possible. The ambiguous samples were not classified randomly: the monkey interpreted the samples differently during different sessions. The interpretation of the ambiguous sample was, in turn, highly correlated with the normalized response of individual neurons in IT to the ambiguous sample. If an ambiguous sample was interpreted as a particular choice during a session, the response to that ambiguous sample more closely resembled the response to that choice. Identical ambiguous images were interpreted differently during different sessions, and neural responses reflected the differing interpretations of the image during that session. The relationship between the interpretation of the image and neural responses strengthened over the course of a session because neural responses shifted to more closely resemble the response to the initial interpretation of the image. The data support a flexible representation of visual stimuli in higher visual areas.

Neural selectivity in anterior inferotemporal cortex for morphed photographic images during behavioral classification or fixation.

Anterior inferotemporal cortex (aIT) contributes to the ability to discriminate and classify complex images. To determine whether and what proportion of single neurons in aIT cortex can yield enough information to classify complex images, we recorded from aIT neurons during the presentation of morphed photographic images in sessions in which monkeys classified images in a two alternative forced-choice--delayed-match-to-sample (2AFC-DMS) task or in sessions in which they performed a fixation task. The sample stimuli were chosen from a sequence in which one image was gradually morphed into another in a pair, while the original pair of images served as choices. Responses of many individual neurons in aIT cortex during the behavioral classification of the images, decoded using an ideal observer analysis, were sufficiently selective to account for the observed behavioral classification of the images. The responses of a separate population of neurons in aIT cortex recorded in subsequent sessions while the monkeys viewed the same images, were less selective than neural responses measured during sessions in which the 2AFC-DMS task was performed. Our findings show that many neurons in aIT could provide sensory information sufficient for the classification of images when a 2AFC-DMS task was performed.

Quantitative comparison between neural response in macaque inferotemporal cortex and behavioral discrimination of photographic images.

Inferotemporal (IT) cortex plays a critical role in the primate ability to perceive and discriminate between images, but the relationship between responses of single neurons and behavioral capacities is poorly understood. We studied this relationship by recording from IT neurons while monkeys performed a delayed-match-to-sample task with two images. On each day, two sample images were chosen to maximize the selectivity of the neuron and task difficulty was manipulated by varying sample duration and by masking the sample. On each trial, monkeys reported which of the two sample images was presented. Neural performance was described using an ideal-observer analysis. Across the population, neural and behavioral sensitivity to changes in sample duration were indistinguishable. Neural sensitivity was dependent on epoch used to analyze neural response; maximal neural sensitivity was achieved in the 128-ms epoch that began 85 ms after sample onset. At most sample durations, the epoch that yielded optimal neural performance was longer than the sample duration, suggesting that neural selectivity persisted after the presentation of the mask during performance of the task. A control experiment showed that neural and behavioral performance improved in the absence of the mask. These observations suggest that the responses of individual IT neurons contain sufficient information to allow behavioral discrimination of images in a demanding task.

Selectivity of inferior temporal neurons for realistic pictures predicted by algorithms for image database navigation.

Primates have a remarkable ability to perceive, recognize, and discriminate among the plethora of people, places, and things that they see, and neural selectivity in the primate inferotemporal (IT) cortex is thought to underlie this ability. Here we investigated the relationship between neural response and perception by recording from IT neurons in monkeys while they viewed realistic images. We then compared the similarity of neural responses elicited by images to the quantitative similarity of the images. Image similarity was approximated using several algorithms, two of which were designed to search image databases for perceptually similar images. Some algorithms for image similarity correlated well with human perception, and these algorithms explained part of the stimulus selectivity of IT neurons. Images that elicited similar neural responses were ranked as more similar by these algorithms than images that elicited different neural responses, and images ranked as similar by the algorithms elicited similar responses from neurons. Neural selectivity was predicted more accurately when the reference images for algorithm similarity elicited either very strong or very weak responses from the neuron. The degree to which algorithms for image similarity were correlated with human perception was related to the degree to which algorithms explained the selectivity of IT neurons, providing support for the proposal that the selectivity of IT neurons is related to perceptual similarity of images.