Not so fast: hippocampal amnesia slows word learning despite successful fast mapping

Abstract

The human hippocampus is widely believed to be necessary for the rapid acquisition of new declarative relational memories. However, processes supporting on-line inferential word use ("fast mapping") may also exercise a dissociable learning mechanism and permit rapid word learning without the hippocampus (Sharon et al. (2011) Proc Natl Acad Sci USA 108:1146-1151). We investigated fast mapping in severely amnesic patients with hippocampal damage (N = 4), mildly amnesic patients (N = 6), and healthy comparison participants (N = 10) using on-line measures (eye movements) that reflected ongoing processing. All participants studied unique word-picture associations in two encoding conditions. In the explicit-encoding condition, uncommon items were paired with their names (e.g., "This is a numbat."). In the fast mapping study condition, participants heard an instruction using a novel word (e.g., "Click on the numbat.") while two items were presented (an uncommon target such as a numbat, and a common distracter such as a dog). All groups performed fast mapping well at study, and on-line eye movement measures did not reveal group differences. However, while comparison participants showed robust word learning irrespective of encoding condition, severely amnesic patients showed no evidence of learning after fast mapping or explicit encoding on any behavioral or eye-movement measure. Mildly amnesic patients showed some learning, but performance was unaffected by encoding condition. The findings are consistent with the following propositions: the hippocampus is not essential for on-line fast mapping of novel words; but is necessary for the rapid learning of arbitrary relational information irrespective of encoding conditions.

Keywords: hippocampus; lexicon; medial temporal lobe; memory; vocabulary.

Figure 1

Task phases (A) and trial sequence of study (B) and 3AFC recognition (C) phases (labels between B&C are relevant for both). A) Task phase sequence for the protocol (see Experimental Methods and Supporting Information Table S1). B and C) All study and test trials began with central fixation followed by display onset, audio instruction playback (including a critical orienting word), and a response phase. Eye movements were monitored during all trials, and we used the critical target word (crit.) onset event to anchor timecourse analyses of eye movements (see Method and Results). B) Fast mapping (FM) and explicit encoding (EE) study formats were similar, but in the EE study format, only one uncommon item was presented, while in the FM study format, two items were presented and a choice was required. C) 3AFC recognition test format was the same after FM and EE encoding. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Behavioral performance at study (A, left) was similar for all groups, while at test (all others) SA patients showed no learning in either condition. Note that panels are labeled counterclockwise. Bars show group means and whiskers are s.e.m. (*P<0.05; ∼P<0.1). A) Left panel: all participants performed FM well above chance at study, but NC (N = 10) and MA (N = 6) groups performed better than SA patients (N = 4). Right panel: in the 3AFC recognition task, NC and MA groups performed well above chance, but SA patients performed no better than chance and much like the NNC group. Neither EE nor FM study affected recognition in SA patients. B) Left panel: free recall of unfamiliar items was poor for all groups, but the SA and MA groups averaged fewer than one recalled item. Right panel: free recall of familiar items was better than that of unfamiliar items for the NC and MA groups, but SA patients recalled very few items. C) Left panel: cued recall based on a novel visual exemplar of a studied item was performed best by the NC group, while SA patients recalled no words on average. Right panel: adding a verbal cue improved performance of the NC and MA groups, but SA patients were still near floor. Neither EE nor FM encoding affected cued recall. D) Post-test minus pre-test familiarity rating differences. NC and MA participants both reliably increased their familiarity ratings of unfamiliar items, while SA patients did not; EE and FM encoding produced similar results. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

On-line eye-movement measures of all groups were similar during study (A), but differed at 3AFC test (B and C) reflecting learning by some groups. In A,C,&D, points and lines indicate group mean proportion fixation time (PFT) per 500 ms timebin (shading shows 95% confidence intervals); in B, bars show group means of fixation counts and whiskers show s.e.m. (*: adjacent bars differed at P < 0.05). C and D plot the same data in different ways to emphasize specific patterns of viewing over time. A) During correct FM study trials, a selection effect was evident for all groups: viewing of the selected target increased after playback of the critical word. B) During 3AFC test trials, differences in fixation (after critical word onset) of nonselected items corresponded to better memory. All groups fixated selected items equally often (center right), whether those items were correctly-selected targets or incorrectly-selected competitors. However, the NC and MA groups fixated non-selected items more in incorrect trials (far right), potentially reflecting uncertainty in recognition processes. Meanwhile, all groups fixated correctly-selected target items (numerically) more than competitors in correct trials (far left), but in incorrect trials incorrectly-selected competitors were fixated as frequently as all non-selected items combined (center left). C) Increased viewing of targets by NC and MA participants at test appeared to be an on-line expression of prior learning. PFT is plotted to targets and competitors in 3AFC test displays before and after the critical word during correct (left) and incorrect (right) trials (group labels on left ordinate). Correct trials: All groups viewed selected target items (black) more later in the trial. Incorrect trials: The SA and NNC groups also steadily increased viewing of an incorrectly-selected competitor item (gray) later in incorrect trials. However, the NC and MA groups differed, showing increased viewing of non-selected items later in the trial, particularly the non-selected target (red). In these groups, memory appeared to modulate the on-line selection effect. D) Knowledge increased viewing of target items versus competitors whether selected or not. NC and MA groups showed a temporally-localized increase in proportion fixation time to selected targets (black) versus selected competitors (gray) (left). SA patients did not exhibit any differences in PFT for correct and incorrect selection (*: PFT Target>PFT Comp., P <0.05). Meanwhile, NC and MA groups viewed non-selected targets more than non-selected competitors (right), reflecting prior learning from FM and EE study trials (*: PFT Target/Comp. Miss>PFT Comp. Hit, P<0.05). A similar pattern in the NNC group may be attributable to within-test learning. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 4

Neuropsychological measures of memory were positively correlated with 3AFC performance in amnesic patients after both FM and EE study. Correlations were calculated between several neuropsychological measures (normalized within a combined SA/MA group) and 3AFC task performance in the FM and EE conditions. Best-fit slopes and correlation coefficients are shown in black for FM and in gray for EE. The top and middle rows incorporate neuropsychological measures related to declarative memory, and correlation coefficients were uniformly positive, frequently significant (*P<0.05), and did not differ between FM and EE study conditions. The bottom row incorporates measures not thought to be related to declarative memory, none of which were significantly correlated with 3AFC task performance. This pattern suggests that word learning may be supported by typical declarative memory mechanisms.