Midbrain activity shapes high-level visual properties in the primate temporal cortex

Abstract

Recent fMRI experiments identified an attention-related region in the macaque temporal cortex, here called the floor of the superior temporal sulcus (fSTS), as the primary cortical target of superior colliculus (SC) activity. However, it remains unclear which aspects of attention are processed by fSTS neurons and how or why these might depend on SC activity. Here, we show that SC inactivation decreases attentional modulations in fSTS neurons by increasing their activity for ignored stimuli in addition to decreasing their activity for attended stimuli. Neurons in the fSTS also exhibit event-related activity during attention tasks linked to detection performance, and this link is eliminated during SC inactivation. Finally, fSTS neurons respond selectively to particular visual objects, and this selectivity is reduced markedly during SC inactivation. These diverse, high-level properties of fSTS neurons all involve visual signals that carry behavioral relevance. Their dependence on SC activity could reflect a circuit that prioritizes cortical processing of events detected subcortically.

Keywords: attentional modulation; change detection; detection activity; object recognition; object selectivity; selective attention; subcortical pathways; superior colliculus; superior temporal sulcus; temporal cortex.

Figure 1.. Identification of the fSTS region as dependent on SC activity

a. Top: Red cue instructed monkey to attend motion stimuli and report changes in motion direction (Δ). Bottom: response rates for left and right Δ (hits) and “no-Δ” (catch) trials. Individual sessions are plotted over gray box indicating mean ± sd. b. Top: Black cue instructed monkey to ignore motion-changes and report a dim in fixation spot. Bottom: response rates for left and right Δ (false alarms) and for dim (hits). Same format as a. c. Functional activations with and without SC inactivation identified a circumscribed region (blue colored patch outlined in white) in fSTS whose modulation was the most dependent on SC activity. d. Coronal slices of the fSTS are overlaid with average attention-related modulation (measured as AUC, see Methods) across neurons recorded in each location (colored spots). Oblique lines indicate electrode approach. Bottom: Example neuronal responses to Attend and Ignore conditions and their corresponding modulation values (gray text), from three recording locations exhibiting poor (left example), good (center), and intermediate (right) attention-related modulations.

Figure 2.. Attention-related modulation in fSTS depends on SC activity

a, b. Population average of the normalized responses to motion stimulus in Attend and Ignore conditions before (a) and during (b) SC inactivation. Error bars indicate 68.2% CI. Grey window indicates time period used for computing attention-related modulation. c. Distribution of attention-related modulation values across neurons before (median = 0.57) and during SC inactivation (median = 0.54). Solid and dotted lines indicate median and no modulation, respectively. Colored shading indicates significance for individual neurons (p < 0.05, bootstrap test). d. Average attention-related modulation across simultaneously recorded neurons within a session (mean ± sd = 23.75 ± 8.72), before and during SC inactivation. See also figures S1–S5.

Figure 3.. Change-evoked activity in fSTS neurons depends on SC activity

a, b. Population average of the normalized responses to motion-change (Δ) and no-change (no Δ) events in the Attend condition before (a) and during (b) SC inactivation. No Δ trials were aligned to time-matched Δ trials. Grey window indicates time period used for computing change-related modulation. Error bars: 68.2% CI. c. Distribution of change-related modulation values before (median = 0.56) and during SC inactivation (median = 0.54). Solid and dotted lines indicate median and no modulation, respectively. Colored shading indicates significance for individual neurons (p < 0.05, bootstrap test). d. Effect of SC inactivation on change-related modulation across sessions. See also figure S3.

Figure 4.. Detect probability in fSTS neurons depends on SC activity

a, b. Population average of the normalized responses to successfully detected motion-change (Δ) trials (“hit”) and undetected trials (“miss”) in the Attend condition before (a) and during (b) SC inactivation. Grey window indicates time period used for computing detection-related modulation (i.e. detect probability, see Methods). Error bars: 68.2% CI. c. Distribution of detect probability values before (median = 0.53) and during SC inactivation (median = 0.51). Solid and dotted lines indicate median and no modulation, respectively. Colored shading indicates significance for individual neurons (p < 0.05, bootstrap test). d. Effect of SC inactivation on detect probability across sessions. See also figure S3.

Figure 5.. Effect of SC inactivation on attention-related modulation, change-evoked activity and detect probability in fSTS neurons was not specific to motion stimuli

a. The monkeys’ task was to detect the brief appearance (0.5 s) of a 2^nd order orientation pulse stimulus, that cannot be detected from its motion energy, from a dynamic white noise stimulus. The pulse was constructed by applying a sinusoidal contrast envelope on the white noise stimulus (see Methods). b. Behavioral performance in the task for the attend (left panel) and ignore (right panel) conditions (similar format to figure 1a, b). c-e. Attention-related modulation before and during SC inactivation (same format as figure 2a–c). f-h. Change-related activity before and during SC inactivation (same format as figure 3a–c). i-k. Detect probability before and during SC inactivation (same format as figure 4a–c). See also figure S2.

Figure 6.. Object selectivity in fSTS neurons depends on SC activity

a. Monkeys fixated a central spot while either object, grid-scrambled, or phase-scrambled images were presented. b. Example neurons that responded selectively to individual object images. c. Object selectivity values for individual neurons, sorted by number of objects selective for, before and during SC inactivation. Non-significant (n.s.) selectivity (p > 0.05, bootstrap test) is shown as white. d, e. Population average of normalized responses to the most selective object and the corresponding scrambled object, before (d) and during (e) SC inactivation. Grey window indicates time period used for computing object selectivity. Black bar above abscissa indicates the duration of image presentation. Error bars: 68.2% CI. f. Distribution of object selectivity values before (median = 0.57) and during SC inactivation (median = 0.55). Solid and dotted lines indicate median and no selectivity, respectively. Colored shading indicates significance for individual neurons (p < 0.05, bootstrap test). g. Effect of SC inactivation on object-selectivity across sessions. See also figure S6.

Figure 7.. Effects of SC inactivation on continuously isolated fSTS neurons

a. A paired comparison of attention-related modulation (AUC) before and during SC inactivation in single continuously isolated fSTS neurons (filled circles). Different colors represent statistically significant modulation in ‘before’ vs ‘during’ (see legend; p < 0.05, bootstrap test). The bar plot (inset) compares the proportion of neurons with significant modulation in ‘before’ but not ‘during’ (purple) to those with significant modulation in ‘during’ but not ‘before’ (green). b-d. Same format as in a for change-related (Δ-related) modulation (b), detect probability (c) and object selectivity (d).