Single-Neuron Representation of Memory Strength and Recognition Confidence in Left Human Posterior Parietal Cortex

Abstract

The human posterior parietal cortex (PPC) is thought to contribute to memory retrieval, but little is known about its specific role. We recorded single PPC neurons of two human tetraplegic subjects implanted with microelectrode arrays, who performed a recognition memory task. We found two groups of neurons that signaled memory-based choices. Memory-selective neurons preferred either novel or familiar stimuli, scaled their response as a function of confidence, and signaled subjective choices regardless of truth. Confidence-selective neurons signaled confidence regardless of stimulus familiarity. Memory-selective signals appeared 553 ms after stimulus onset, but before action onset. Neurons also encoded spoken numbers, but these number-tuned neurons did not carry recognition signals. Together, this functional separation reveals action-independent coding of declarative memory-based familiarity and confidence of choices in human PPC. These data suggest that, in addition to sensory-motor integration, a function of human PPC is to utilize memory signals to make choices.

Keywords: confidence; episodic memory; human; memory retrieval; posterior parietal cortex; recognition memory; single neuron.

Figure 1. Task, behavior and electrode location

(A) Task. (B) Behavioral ROC curves for each session (grey) and average (red). (C) z-transformed average ROC curve. (D) Probability of response as a function of ground truth (color). (E) Retrieval accuracy as a function of confidence. (F) Average confidence was higher for correct vs. incorrect responses. (G) Decision time varied as a function of both familiarity (new/old) and confidence. (H-I) True positive rate (H) and confidence (I) of responses to old stimuli during recognition was independent of serial position during learning. (J-K) Location of recording array, illustrated using flatmaps (J) and reconstructed grey matter surfaces (K). Anatomical landmarks indicated are central sulcus (green), postcentral sulcus (red), and the intraparietal sulcus (cyan).

Figure 2. Examples of individual neurons that carry recognition-memory related signals

(A-C) Raster (top) and PSTH (bottom) of three example neurons. Inset shows the average waveform of the neuron. Stimulus onset is at t=0. Colors indicate the stimulus type (old or new) and the confidence indicated by the subject (high or low). Only trials where the subject provided the correct answer (regardless of confidence) are shown. (A-B) Are MS cells of Type 1 (new>old) and Type 2 (old>new), respectively. Note the increase in firing rate for one but not the other trial type (new and old, respectively). (C) Is a confidence coding cell (Type 1, high>low). (D) Average response in a 2s window following stimulus onset for the neurons shown in A-C.

Figure 3. Population summary of recognition memory signals in PPC

A) distribution of memory preference across all recorded neurons. Significant MS neurons (n=166) are indicated in orange, non-significant in blue. The sign of the preference indicates which stimulus each cell preferred (Type 1 vs. Type 2). B) distribution of confidence preference across all recorded neurons. Significant CS neurons (n=130) are indicated in orange, non-significant in blue. The sign of the preference indicates which stimulus each cell preferred (Type 1 vs. Type 2). C) Memory versus confidence preference across the population shows groups of neurons that code stimulus familiarity (red), confidence (green), or both (magenta). E) MS neurons have a significantly positive confidence preference (p=0.0057 for old>new and p=0.0041 for new>old). E) MS neurons provide a stronger memory signal for high compared to low confidence choices (AUC mirror histogram high vs low; p=3.02e-5 all neurons; new>old p=0.014; old>new p=0.00033). F) AUC of high vs. low confidence for each neuron, independently for MS neurons that prefer familiar (red) and novel (blue) stimuli (sign-test; p=0.0023, 102/164 above diagonal). See also Figure S2, S4, and S6.

Figure 4. PPC neurons encode memory-based choices

A) Group PSTH of all MS neurons, pooled according to their preferred and non-preferred stimulus (Pref and NP, respectively). Tuning preference is defined according to ground truth. Note that during error trials, neurons signal according to their non-preferred stimulus (the choice). Also note modulation by confidence only for the preferred, but not non-preferred, trials. B-C) Single-trial analysis confirms choice coding during error trials (Error non-preferred is significantly larger than error preferred p=9e-6; high vs. low confidence p=5e-5). D) Choice (CP) vs. memory (MP) probability for all neurons. E) CP is significantly larger than MP for both new>old (p=5.9e-5, red) and old>new (p=0.008, blue) MS neurons. F) Time-course of CP. G) CP varies as a function of confidence, with more reliable signaling for high confidence responses (1×3 repeated measure ANOVA, F=19.8, p=7.19e-9, n=166). See also Figure S5.

Figure 5. Neurons encode memory strength and not action choices

A) Control task. B) Mean single-trial response shows no strength gradient (p = 0.94 for high (++) versus low (+) confidence responses). C) Time-course of CP does not vary as a function of confidence (1×3 repeated measure ANOVA, F=0.79, p=0.45, n=65). D) Control cells have no confidence preference (p=0.20 and p=0.23, respectively). E) Control cells don't provide more information for high compared to low-confidence decisions (p=0.23). F) Effect size for new vs. old (1-3 vs 4-6) for the control task (x-axis) and the memory task (y-axis). Effect sizes were not correlated (r=-0.04 p=0.82 for NS cells, r=0.16 p=0.36 for MS cells and r=-0.02 p=0.65 for all cells recorded in both tasks) and the same neurons did not differentiate the same choices in the two tasks. Only cells recorded in both tasks are shown. G-H) Population decoding performance in memory (G) and control (H) task. (G) Decoding of confidence was more accurate for high vs. low confidence (p=9e-8). New vs. old decoding was more accurate for high vs. low confidence (p=0.0064). (H) Decoding performance did not differ for decoding confidence (left, p=0.64) and new/old (right, p=0.77). See also Figure S3.

Figure 6. Latency of memory signal

A) cumulative firing rate for MS neurons. B) Difference of cumulative firing rate. First significant point of time was t=553ms. (same analysis for control task: 262ms).