Can Delay-Period Activity Explain Working Memory?

Abstract

Working-memory tasks often lead to elevated delay-period discharge rates in cortical neurons. When this altered neuronal discharge rate, called delay activity, shows stimulus specificity, it is a good candidate for a neuronal mechanism of working memory. If the delay activity is indeed the carrier of memory, then experimental manipulation during the delay period that disrupts delay activity should also disrupt behavioral performance. We tested this hypothesis in two macaque monkeys with a delayed matching-to-sample task (delay time: 8 or 10 s) in which only two visual images were used. In each trial, one of the images was randomly chosen as the sample. In control trials (without disruptive stimulation), the monkeys performed at the level of 74.3% correct recognition. Three electrical stimulation levels (mild: a 0.25-s train of electrical pulses; medium: 1-s train; strong: 4 s), delivered to the hippocampal formation or to the orbito-frontal and inferotemporal cortices during delay period, decreased the performance to 71.4, 66.8, and 58.0% respectively (all are significantly less than control performance, P < 0.05 for mild stimulation and P < 0.0001 for other stimulation levels). Three hundred and thirty-four cells were recorded from inferotemporal (211 cells) and prefrontal (123 cells) cortices. Significant (P < 0.05) stimulus-specific delay activity was found in about one-third of recorded cells. For these cells in control trials, the mean difference in delay-period spike rates between preferred and nonpreferred images was 26%. The electrical stimulation reduced this difference to 20% (not a statistically significant reduction) in trials with mild stimulation, to 14% (P < 0.05) with medium stimulation, and just to 4% (P < 0.0005) with strong stimulation. These results, that increasing electrical stimulation reduced neuronal selectivity and at the same time reduced behavioral performance, directly support the hypothesis that delay activity is the carrier of memory through the delay period.

Oscillatory multiplexing of neural population codes for interval timing and working memory

“…Sound frequency information (i.e., pitch) is parametrically maintained by the firing rates of primate PFC neurons during the delay period (e.g., high pitch stimuli produce high spike rates-e.g., Brody et al, 2003;Romo et al, 1999). Evoked or spontaneous disruptions of these sustained activities are correlated with the failure of maintenance (e.g., Fuster, 1973;Quintana et al, 1988;Sobotka et al, 2005;Wang et al, 2011), supporting the importance of sustained neural activity during the delay periods for the maintenance of information in working memory.…”

Enhancement of Object Representations in Primate Perirhinal Cortex During a Visual Working-Memory Task

“…In addition to long-term memory, working memory within temporal cortex has been the subject of monkey studies (Baylis and Rolls 1987;Davachi and Goldman-Rakic 2001;Eskandar et al 1992;Fuster 1990;Fuster and Jervey 1981;Holscher and Rolls 2002;Miller and Desimone 1994;Miller et al 1991;Miyashita and Chang 1988;Nakamura and Kubota 1995;Sobotka et al 2005). Working memory is believed to be closely related to attention (Awh and Jonides 2001;Awh et al 2006;Barnes et al 2001;de Fockert et al 2001;Desimone 1996).…”

Retrieval Attempts Transiently Interfere with Concurrent Encoding of Episodic Memories But Not Vice Versa

“…Similarly, the effect of SOA between hippocampal ES and the presentation of retrieval cues, using the present three-phase dual-task paradigm, could reveal much about the dynamic interdependence of encoding and retrieval activities within the hippocampus. Sobotka et al (2005) also showed recently that delay-interval ES directly in the monkey hippocampus, persisting for 125-250 ms but delivered 1 s after onset of the sample stimulus, disrupts recognition in a short-term delayed matching-to-sample task. Their findings, in conjunction with our own and those of Coleshill et al (2004), suggest that the hippocampus may be differentially engaged, or controlled, in long-term versus short-term (working) memory tasks.…”