Robust habit learning in the absence of awareness and independent of the medial temporal lobe

Abstract

Habit memory is thought to involve slowly acquired associations between stimuli and responses and to depend on the basal ganglia. Habit memory has been well studied in experimental animals but is poorly understood in humans because of their strong tendency to acquire information as conscious (declarative) knowledge. Here we show that humans have a robust capacity for gradual trial-and-error learning that operates outside awareness for what is learned and independently of the medial temporal lobe. We tested two patients with large medial temporal lobe lesions and no capacity for declarative memory. Both patients gradually acquired a standard eight-pair object discrimination task over many weeks but at the start of each session could not describe the task, the instructions or the objects. The acquired knowledge was rigidly organized, and performance collapsed when the task format was altered.

Figure 1. Magnetic resonance images showing the extent of damage to the temporal lobe in amnesic patients

Images are shown for patient EP (a) and patient GP (b). The first three images in each row are T₂-weighted axial images through the temporal lobe. The images are continuous 5-mm sections (with 2.5-mm gaps) and are arranged from ventral to dorsal (left to right). Damaged tissue is indicated by a bright signal. The last image in each row is a coronal T₁-weighted image at the level of the amygdala. Damaged tissue is indicated by a dark signal. See ref. and Supplementary Information for a detailed description of the lesions.

Figure 2. Performance on the concurrent discrimination task

a, Controls (n = 4) learned the task easily within three sessions and performed well on the sorting task 3–6 days later (grey bar). The black bar shows performance immediately afterwards when participants were asked to verbalize their choices rather than reach for objects. Results are means ± s.e.m. b, EP gradually learned the object pairs across 18 weeks. Five days later, he failed the sorting task (grey bar) but then, immediately afterwards, performed well in the standard task format while verbalizing his responses (black bar). Seventeen days later, EP again failed the sorting task (grey bar) but performed perfectly when 40 trials were given exactly as in original training (white bar). c, GP learned the object pairs gradually during 14 weeks. Like EP, he failed the sorting task on two different occasions, 5 days after training and again 17 days later. In both instances he performed well immediately afterwards when the original task format was reinstated (black bar, verbalizing; white bar, standard task). The dashed line indicates the results expected by chance.