Neurons in macaque inferior temporal cortex show no surprise response to deviants in visual oddball sequences

Abstract

Many studies measured neural responses in oddball paradigms, showing a different response to the same stimulus when presented with a low (deviant) compared with a high probability (standard) in a sequence. Such a differential response is manifested in event-related potential studies as the mismatch negativity (MMN) and has been observed in several sensory modalities, including vision. Other studies showed that stimulus repetition suppresses the neural response. It has been suggested that this adaptation effect underlies the smaller responses to the standard compared with the deviant stimulus in oddball sequences. However, the MMN may also reflect the violation of a prediction based on the sequence of standards, i.e., a surprise response. We examined the presence of a surprise response to deviants in visual oddball sequences in macaque (Macaca mulatta) inferior temporal (IT) cortex, a higher-order cortical area. In agreement with visual MMN studies, single-unit IT responses were greater for the deviant than for the standard stimuli. However, single IT neurons showed no greater response to the deviant stimulus in the oddball sequence than to the same stimulus presented with the same probability in a sequence that consisted of many stimuli. LFPs also showed no evidence of a surprise response. These data suggest that stimulus-specific adaptation, without a surprise-related boost of activity to the deviant, underlies the responses in visual oddball sequences even in higher visual cortex. Furthermore, we show that for IT neurons such adaptive mechanisms take into account a relatively short stimulus history, with weaker effects at longer time scales.

Keywords: adaptation; inferior temporal cortex; macaque; mismatch negativity; repetition suppression; surprise response.

Figure 1.

Visual oddball test. Two selected stimuli (A and B) were presented randomly interleaved in blocks of 100 or 300 presentations, with each stimulus being presented either frequently (probability 0.90, standard) or rarely (probability 0.10, deviant) within a block (oddball sequences). In addition, the two stimuli A and B were also presented with the same probability (reference), being randomly interleaved with eight weakly effective stimuli in the equiprobable sequence. When fixating on a red target square (here shown not to scale), monkeys were continuously presented a sequence of stimuli, with each stimulus being presented for 300 ms and followed by a 300-ms-long blank screen. The stimuli A and B differed between neurons and were selected based on responses in a search test.

Figure 2.

Effect of stimulus condition on the spiking activity for the natural stimuli. A, B, Population peristimulus time histograms for the natural stimuli for Monkeys P (A) and K (B) in the main test (blocks of 100 stimulus presentations). Standard, Standard stimulus in oddball sequence; Deviant, the same stimulus presented as a deviant in the other oddball sequence; Reference, the same stimulus presented in the equiprobable condition. N denotes the number of analyzed stimulus × neuron combinations. Stippled vertical lines indicate stimulus onset and offset. Bin width is 10 ms. Mean activity is plotted at the center of the corresponding time bins (e.g., response at 0 ms, stimulus onset, corresponds to the mean response in a time window from −5 to 5 ms). (C, D) Distribution of the D_S indices (comparing the responses to a stimulus presented as a deviant and as a standard; positive values indicate a higher response to a deviant compared with a standard stimulus) for the same stimulus × neuron combinations as in A, B for Monkeys P (C) and K (D). E, F, Distribution of the D_R indices (comparing the responses to a stimulus presented as a deviant and as a reference; positive values indicate a higher response to a deviant compared with a reference stimulus) for the same stimulus × neuron combinations as in A, B for Monkeys P (E) and K (F). Median values are indicated by an arrow.

Figure 3.

Effect of stimulus condition on the spiking activity for the face stimuli. A, Face stimulus set. The two boxes indicate the frontal and profile views of a female face. Such a pair of stimuli would be presented, when selected based on a search test, in the oddball and equiprobable sequences of 100 presentations. B, Population peristimulus time histogram for the face stimuli. N denotes the number of analyzed stimulus × neuron combinations. Same conventions as in Figure 2A.

Figure 4.

Effect of the difference in response to the two probe-stimuli A and B (B_W index) on the response in oddball and equiprobable sequences. A, D_R index plotted as a function of the B_W index for each of the 113 neurons tested in the main test (100 stimulus presentations per block) for both monkeys and stimulus sets. Each point corresponds to the D_R value for one of the two stimuli (A or B) to which a neuron responded best when presented as a reference. The linear regression line is indicated in red. B, Population peristimulus time histograms for the 25 neurons with a B_W index ≤0.1 (A, left pair vertical stippled lines). C, Population peristimulus time histograms for the 27 neurons with a B_W index larger or equal to 0.9 (A, right vertical stippled lines). Same conventions as in Figure 2A.

Figure 5.

Effect of presentation order within a block of stimuli on the response for the three stimulus conditions. A, The time course of the average population response to a stimulus within a block (sequence of 100 stimulus presentations) plotted for each condition separately. Data of the analyzed stimulus × neuron combinations (N = 207) are pooled across both monkeys and stimulus sets. Note that the number of data points for each presentation order varies across stimulus conditions. The stippled curves correspond to fits of the time courses with a polynomial inverse first order function. B, Population peristimulus time histograms of the mean responses for the three conditions of the 27 neurons for which B_W ≥ 0.9 and this for the last 25% of the stimulus presentations of a block (presentation order 76–100). Same conventions as in Figure 2A.

Figure 6.

Spiking activity within blocks of 300 stimulus presentations. A, Population peristimulus time histograms of the responses for the three stimulus conditions, averaged across the presentations of the whole block of stimuli. B, C, Population peristimulus time histograms of the responses for the three stimulus conditions, averaged across the first 100 (B) or the last 100 presentations (C) of the 300-presentation-long blocks. Data obtained in Monkey P (43 stimulus × neuron combinations). Same conventions as in Figure 2A.

Figure 7.

Effect of stimulus history on spiking responses to a stimulus in oddball sequences. Tree diagrams show the mean normalized response (and bootstrapped 95% confidence intervals) to a stimulus, presented as a standard (high probability presentations; A) or a deviant (low probability presentations; B), as a function of the local history in that sequence. The responses are plotted as a function of sequence order, i.e., the number of stimuli taken into account to define the sequence. The local stimulus history is indicated for each averaged response (e.g., BA corresponds to the response to stimulus A following B, ABBA corresponds to the response to stimulus A following the sequence ABB etc.). Green symbols indicate responses to A in sequences where the first stimulus of that short sequence was the same, i.e., A, whereas red symbols indicate responses to A in sequences where the first stimulus was different, i.e., B. Green lines connect sequences of which the higher-order sequence starts with A, i.e., is identical to the stimulus for which the response is averaged, whereas red lines connect sequences of which the higher-order sequence starts with B. Only averages of at least 100 unaborted stimulus sequences are shown. Data were obtained in the main test.

Figure 8.

Effect of fixation breaks on spiking activity for the three stimulus conditions (main test; blocks of 100 stimulus presentations). A, The mean response to the standard before (red) and after a fixation break (green) as a function of the fixation break duration (running average with width of a boxcar kernel of 500 ms with a step of 10 ms) for all standards that were followed by a fixation break, pooled across all analyzed stimulus × neuron combinations of both monkeys and stimulus sets. The blue curve indicates the mean responses to the first presentation of the standard for the same blocks of stimuli as those of the other curves. Note that the sample sizes were smaller for the longer fixation break durations. B, The mean responses to a stimulus presentation for each unaborted sequence plotted as a function of the presentation order within that unaborted sequence, with presentation order 1 corresponding to the presentation of the stimulus immediately after a fixation break. For the standard condition (red), the responses to all standards were averaged as a function of their presentation order. For the deviant condition (green), the responses to deviants were averaged as a function of the number of preceding standards in that unaborted sequence. Thus, a mean response to a deviant or a standard at presentation order 3 corresponds to the response to a deviant or standard, respectively, following two presentations of the standard stimulus after a fixation break. The responses to the same stimuli presented as a reference (blue) were averaged as a function of their presentation order within unaborted sequences of the equiprobable condition. Averaging was first performed for each analyzed stimulus × neuron combination and then across all analyzed stimulus × neuron combinations. The data of both monkeys and stimulus sets were pooled. Only averages of at least 50 stimulus × neuron combinations are plotted. Bands indicate SEM.

Figure 9.

LFP power for the three stimulus conditions in oddball and equiprobable sequences (main test; 100-presentation-long sequences). Mean normalized power (and SEM; averaged across the two probe-stimuli) for each stimulus condition (standard, open bars; deviant, light gray bars; reference, dark gray bars), time × frequency analysis window (rows) and combination of monkey and stimulus set (columns). The time × frequency analysis window for a row is given above the row. N denotes the number of analyzed stimulus × site combinations. Note that the scale along the y-axis varies across different panels.