Unconscious relational encoding depends on hippocampus

Abstract

Textbooks divide between human memory systems based on consciousness. Hippocampus is thought to support only conscious encoding, while neocortex supports both conscious and unconscious encoding. We tested whether processing modes, not consciousness, divide between memory systems in three neuroimaging experiments with 11 amnesic patients (mean age=45.55 years, standard deviation=8.74, range=23-60) and 11 matched healthy control subjects. Examined processing modes were single item versus relational encoding with only relational encoding hypothesized to depend on hippocampus. Participants encoded and later retrieved either single words or new relations between words. Consciousness of encoding was excluded by subliminal (invisible) word presentation. Amnesic patients and controls performed equally well on the single item task activating prefrontal cortex. But only the controls succeeded on the relational task activating the hippocampus, while amnesic patients failed as a group. Hence, unconscious relational encoding, but not unconscious single item encoding, depended on hippocampus. Yet, three patients performed normally on unconscious relational encoding in spite of amnesia capitalizing on spared hippocampal tissue and connections to language cortex. This pattern of results suggests that processing modes divide between memory systems, while consciousness divides between levels of function within a memory system.

Keywords: flexible; implicit; nondeclarative; relational; subliminal.

Figure 1

Study overview. There were three sessions that took place on three half-days. In the first session, we examined patients and controls neuropsychologically. The second and third sessions were devoted to experimentation. Depending on a participant’s MRI compatibility, the two experimental sessions were conducted in the magnetic resonance scanner or in a behavioural laboratory. The second session started with anatomical MRI and ended with arterial spin labelling. In-between these scans, participants performed the functional MRI (fMRI) experiment on unconscious relational memory with one encoding trial and the functional MRI experiment on unconscious single word memory (semantic word priming). The third session started with the resting state functional MRI scan followed by the functional MRI experiment on unconscious relational memory with nine encoding trials. This session ended with the objective tests of stimulus awareness (Supplementary material).

Figure 2

Designs of the three memory functional MRI experiments. (A) Relational memory. Participants performed two functional MRI experiments on unconscious relational encoding and retrieval. These experiments had similar designs but one experiment had a single encoding trial and the other nine. For subliminal encoding, we presented masked pairs of unrelated nouns, while participants performed an attention task. Encoding and retrieval were separated by 5 min of quiet rest. For unconscious retrieval, we presented participants with supraliminal (visible) word pairs. Nouns in these pairs were semantic neighbours of subliminal encoding nouns. Combinations of superordinate concepts and hence semantic relations were retained from study to test in ‘intact pairs’, while superordinate concepts were recombined and semantic relations broken in ‘broken pairs’. Because the study and test format differed in this task, flexibility of memory representation was required. The indirect retrieval task was to decide whether the two nouns in a pair fit together semantically or not. (B) Single word memory. One trial comprised the subliminal (masked) presentation of a noun that was immediately followed by a supraliminal (visible) noun. Subliminal and supraliminal nouns were either related semantically or unrelated. Participants engaged in an attention task during subliminal presentations and gave subjective pleasant-unpleasant judgments to supraliminal nouns. Due to the repetition of superordinate concepts (but not stimuli), semantic priming can be expected in the ‘related’ condition. t = time.

Figure 3

Behavioural results. (A) Unconscious relational retrieval. Displayed is the percentage of fit responses given to intact and broken word pairs at test. Controls (n = 11), but not amnesic patients (n = 11), gave significantly more fit responses to intact than broken word pairs; they needed nine encoding trials for this result. *P < 0.05. (B) Conscious and unconscious verbal relational encoding and retrieval were marginally correlated, which is consistent with the view that the hippocampal memory system serves both conscious and unconscious encoding/retrieval. This was true for the entire sample consisting of controls and patients (n = 22; r = 0.349, P_one-tailed = 0.056) and for the patients alone (n = 11; r = 0.442, P_one-tailed = 0.087). (C) Unconscious relational memory dissociates from unconscious single word memory. We tested for the stochastic independence of unconscious single word memory (Δ mean RTs in ms to related versus unrelated supraliminal words) and unconscious relational memory (Δ % of fit responses to intact versus broken pairs following 9-trial encoding) by computing two regression analyses using each type of retrieval performance to predict the other. Single word memory was not correlated with relational memory (all participants, n = 22, r = −0.176, P = 0.432). Intercepts in both regression analyses were significant, which indicates that performance on each type of memory was still significantly above chance if performance on the other type of memory was at chance level. n.s. = not significant. RT = reaction time.

Figure 4

Brain activity associated with unconscious relational encoding and retrieval. The three well performing patients (Patients 4, 5 and 6) exhibited hippocampal activity changes during unconscious relational encoding and retrieval. Each and every patient contributed to the displayed group effects in hippocampus. For this analysis, we thresholded each patient’s individual contrasts with P = 0.05, uncorrected. Functional MRI data are depicted on coronal slices; the corresponding MNI y-coordinates are indicated.

Figure 5

Resting state functional connectivity. Results of the independent component analyses performed on the resting state functional MRI data are depicted in axial slices at MNI z = −24 to −12 in steps of 4 mm. Independent component analyses were performed separately for each participant. The resulting images reflect the degree to which the component that is most prominent in the hippocampus contributes to the signal in other parts of the brain. Z-transformed images were averaged across groups of interest (controls, n = 11; well performing patients, n = 3; MRI-compatible subgroup of the group of poorly performing patients, n = 3).