Phase of firing does not reflect temporal order in sequence memory of humans and recurrent neural networks

The temporal order of a sequence of events has been thought to be reflected in the ordered firing of neurons at different phases of theta oscillations. Here we assess this by measuring single neuron activity (1,420 neurons) and local field potentials (921 channels) in the medial temporal lobe of 16 patients with epilepsy performing a working-memory task for temporal order. During memory maintenance, we observe theta oscillations, preferential firing of single neurons to theta phase and a close relationship between phase of firing and item position. However, the firing order did not match item order. Training recurrent neural networks to perform an analogous task, we also show the generation of theta oscillations, theta phase-dependent firing related to item position and, again, no match between firing and item order. Rather, our results suggest a mechanistic link between phase order, stimulus timing and oscillation frequency. In both biological and artificial neural networks, we provide evidence supporting the role of phase of firing in working-memory processing.

学界普遍认为，事件序列的时序结构可通过神经元在θ振荡（theta oscillations）不同相位下的有序放电行为得以反映。本研究通过对16名执行时序工作记忆任务的癫痫患者的内侧颞叶进行神经记录，测定了1420个单个神经元的活动与921通道的局部场电位（local field potentials），以此验证上述假说。在记忆维持阶段，我们观测到θ振荡现象、单个神经元对θ相位的倾向性放电，以及放电相位与记忆项目位置之间的密切关联。然而，神经元的放电时序与记忆项目的呈现顺序并不一致。我们通过训练循环神经网络（recurrent neural networks）完成同类任务，同样观测到了θ振荡的产生、与项目位置相关的θ相位依赖性放电，且再次出现了放电时序与项目顺序不匹配的情况。相较之下，本研究结果揭示了相位顺序、刺激时序与振荡频率三者间的机制性关联。无论是生物神经网络还是人工神经网络场景下，本研究均提供了证据支持放电相位在工作记忆加工中的作用。