A classic distinction from the domain of external attention is that between anticipatory orienting and subsequent re-orienting of attention to unexpected events. Whether and how humans also re-orient attention ‘in mind’ following expected and unexpected working-memory tests remains elusive. We leveraged spatial modulations in neural activity and gaze to isolate re-orienting within the spatial layout of visual working memory following central memory tests of certain, expected, or unexpected mnemonic content. Besides internal orienting after predictive cues, we unveil a second stage of internal attentional deployment following both expected and unexpected memory tests. Following expected tests, internal attentional deployment was not contingent on prior orienting, suggesting an additional verification – ‘double checking’ – in memory. Following unexpected tests, re-focusing of alternative memory content was prolonged. This brings attentional re-orienting to the domain of working memory and underscores how memory tests can invoke either a verification or a revision of our internal focus.

Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here, we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions—the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS)—while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal’s choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.