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The main character of Whisper of the Heart is a girl named Shizuku Tsukishima who is in junior high school in a small town near Tama in West Tokyo. She loves reading and writing in her spare time, but her parents wish she would pay more attention to her schoolwork and her upcoming high-school entrance exams.
One day Shizuku sees a cat riding on the train with her. She follows the cat off the train and ends up at an unusual little curiousity shop. She meets the shop's owner, a kindly old man.
Outside the shop, Shizuku finds Seiji Amasawa, a boy from her school whose name she had first noticed on the cards of her library books: he had checked out all of the same books before she did. The shopkeeper is Seiji's grandfather. Seiji and Shizuku's first encounters are brief and uncomfortable, but eventually they grow close to one another. Shizuku learns that Seiji is working to become a violin-maker. Ashamed that she has no similar aspirations, Shizuku dedicates herself to writing, but abandons her studies and falls farther behind at school.
When Seiji leaves for Italy to begin a trial apprenticeship with an instrument-maker, Seiji's grandfather helps encourage Shizuku to complete her ambitious writing project. The movie's resolution comes as Shizuku finishes her story and decides to resume her schoolwork; Seiji returns from his first stay in Italy; and Seiji and Shizuku declare their love for each other.
In the film, Shizuku translates the song "Country Road" (originally performed by Olivia Newton John) into Japanese for her school's chorus club. She also writes her own Japanese version of the song, called "Concrete Road," about her hometown in western Tokyo. These songs play a role at various points in the story.
The cat in Whisper of the Heart is called "Moon" or "Muta" by different characters, and appears again in another Studio Ghibli film, The Cat Returns.
Many consider Whisper of the Heart to be similar in theme to Kiki's Delivery Service, also by Studio Ghibli.